- Email: [email protected]
Standards and Guidelines for Technologists Performing Central Dual-Energy X-Ray Absorptiometry
Journal of Clinical Densitometry, vol. 10, no. 2, 189e195, 2007 Ó Copyright 2007 by The International Society for Clinical Densitometry 1094-6950/07/10:189e195/$32.00 DOI: 10.1016/j.jocd.2007.01.005
ISCD Canadian Standards
Standards and Guidelines for Technologists Performing Central Dual-Energy X-Ray Absorptiometry Aliya A. Khan,*,1 Anita Colquhoun,2 David A. Hanley,3 Lawrence G. Jankowski,4 Robert G. Josse,5 David L. Kendler,6 Brian Lentle,6 William D. Leslie,7 E. Michael Lewiecki,8 Elaine O’Neill,9 Stephen Robertson,10 Zeba A. Syed,11 S. Bobo Tanner,12 and Dave Webster13 1
Divisions of Endocrinology and Geriatrics, McMaster University, Hamilton, Ontario, Canada; 2Osteoporosis Program, Women’s College Hospital, Toronto, Ontario, Canada; 3Department of Medicine, University of Calgary, Calgary, Alberta, Canada; 4Illinois Bone and Joint Institute, Morton Grove, IL; 5St. Michael’s Osteoporosis Centre, University of Toronto, Toronto, Ontario, Canada; 6University of British Columbia, Vancouver, British Columbia, Canada; 7Departments of Medicine and Radiology, University of Manitoba, Manitoba, Canada; 8New Mexico Clinical Research & Osteoporosis Center, Albuquerque, NM; 9Halton Healthcare Services, Oakville Hospital, Halton, Ontario, Canada; 10Prohealth Clinical Research, Vancouver, British Columbia, Canada; 11Musculoskeletal Radiology, Hanover Hospital, Hanover, PA; 12 Divisions of Rheumatology and Allergy, Vanderbilt University, Nashville, TN; and 13Sudbury Regional Hospital, Sudbury, Ontario, Canada
Key Words: Bone density; osteoporosis; standards; technologist.
that a technologist adheres to essential elements of the bone density examination. As an important sequel to the Canadian Standards for physicians, this document details what technologists must do to produce quality bone densitometry results. The primary objectives of the ISCD are to promote education and ensure standardization of densitometry, so as to improve patient care for osteoporosis and metabolic bone disease. Each densitometry facility needs to develop its own guidelines to ensure optimal quality bone densitometry results. Although these guidelines may vary from one facility to the next, standard features common to all DXA testing are needed to ensure that appropriate information is supplied to referring physicians. In this document, we suggest standards for developing standard operating procedures, to be used in conjunction with the manufacturer’s recommendations for instrument maintenance and operation. In this paper, we will discuss all of the aspects of bone densitometry relevant to technologists, reviewing issues of relevance to all DXA manufacturers and not specific to individual technologies. These features include issues of quality
Introduction Standards of care from the Canadian Panel of the International Society for Clinical Densitometry (ISCD) have been developed to improve the quality of bone densitometry practice across Canada. This document follows Standards 1 and 2 previously published by the Canadian Panel (1,2). Optimizing technologist standards is a critical component of providing Canadians with high-quality bone density testing by dual-energy X-ray absorptiometry (DXA). Achieving high-precision bone mineral density (BMD) scans requires Received 11/08/06; Revised 01/10/07; Accepted 01/12/07. This document was created by the ISCD Canadian Regional Panel. The ISCD has approved this document as being relevant to local or regional needs and does not necessarily represent official ISCD positions or ISCD positions as they relate to this specific jurisdiction. *Address correspondence to: Aliya A. Khan, MD, FRCPC, FACP, Professor of Clinical Medicine, Divisions Endocrinology and Geriatrics, McMaster University, 209-331 Sheddon Avenue, Oakville, Ontario L6J 1X8, Canada. E-mail: [email protected]
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190 assurance (QA), precision assessment, scan acquisition, scan analysis, and special circumstances. By applying standardized bone densitometry procedures, the quality of bone density scanning and patient care in Canada likely will improve greatly.
Scan Preparation and Setup Facilities need to adhere to a standardized approach to scanning to maintain diagnostic accuracy and reduce variability on serial scanning. As a general rule, technologists are advised to perform scans of at least two relevant skeletal sites. By doing so, if patients have features precluding analysis at any one site, a second valid site still is available for testing. Both the spine and hip should be scanned, whenever possible. If either site does not provide a valid result, then the forearm can be used as the second site. The contralateral (opposite) side should be scanned, if there is a history of previous fracture or surgery affecting the hip or forearm.
Patient Preparation for the Scan After having the patient remove footwear, an accurate height and weight must be obtained. For height measurement, hair should be flattened. Because height is such an important indicator of spinal compression fracture, stadiometric measurements should be used if possible. If a stadiometer is unavailable, a wall-mounted tape measure may be the next best option. Alternatively, a carpenter’s level on the horizontal arm of the scales measuring device will improve the precision of measurement on doctor’s office scales. The patient should be asked if there is a chance of pregnancy and, if pregnancy cannot be excluded, the scan must be delayed and the 10-d rule should be followed. Although recent pregnancy and breastfeeding are not contraindications to bone density testing, these produce transient, reversible changes in bone mass and therefore BMD testing ideally should be delayed for 6 mo postpartum (3e5). A scan also may need to be delayed if (1) a calcium supplement has been swallowed within 2 h, or (2) a radioactive isotope has been administered within 72 h (even longer when isotopes with long half-lives, such as iodine-131, indium-111, or gallium-67, have been used). Generally, in such circumstances, one should delay for 10e12 half-lives. A delay of 14 d is recommended if the patient has had a radiographic procedure involving contrast material. All metal overlying the scan area should be removed. If the metal on the clothing is not easily pushed aside, clothing should be removed and the patient gowned. (It often helps to ask each patient to wear a loose jogging suit to the densitometry session.) The patient then should lie comfortably on the scanning table, breathing normally. Patient biographical information must be entered carefully. Errors in this information will have important consequences, aside from misidentification of the patient. Sex assignment errors will affect the calculations of T-score and Z-score. Depending on the manufacturer, the patient’s race and weight also can affect both the T-score and Z-score. The ISCD Journal of Clinical Densitometry
Khan et al. recommends using a nonerace-adjusted (White) reference population database for all T-score calculations. Z-scores should be race-adjusted, where suitable reference data exist. For the purpose of Z-score calculations, the patient’s selfreported ethnicity should be used. Patient weight may affect the Z-score calculation when this software option is enabled, but the ISCD recommends against weight-adjusting the Z-score. The biography always should be updated on rescanning.
Scan Acquisition Scan mode may be chosen by machine default, but should be overridden by the operator if there are valid reasons to do so (e.g., body thickness requiring a slower scan speed). If, during the initial scanning, there is evidence of suboptimal positioning, the scanner should be stopped, the patient repositioned, and the scan restarted. Absolute attention to detail is critical in all aspects of patient positioning, scan acquisition, and analysis to ensure the highest quality densitometry, particularly for comparing serial scans. Proper technique will ensure that the best possible information is available for the reporting physician. BMD reports can significantly affect patient management, both in the initial determination of a patient’s fracture risk and in subsequent follow-up of patients on therapy.
Lumbar Spine The final preparation for a spine scan starts with the patient sitting at the center of the scan table aligned along the long axis of the table. Best positioning is achieved by guiding the patient with support to the supine position centered on the table. The appropriate positioning block must be chosen and placed under the patient’s legs to flatten the lumbar lordosis, according to the manufacturer’s instructions. Properly performed, this will permit easy segmentation of lumbar levels. The block size and orientation should be recorded and used for all follow-up evaluations with that same patient. Position the laser alignment beam 2 cm inferior to the umbilicus or 2 cm inferior to the xyphoid, depending on the manufacturer’s instructions. The scan should include at least part of L5, usually some of the iliac crest, and part of T12 with some rib. The spine must be aligned exactly with the long axis of the table and there must be equal soft tissue on each side of the spine. The presence of scoliosis will present major and often insurmountable problems for positioning.
Hip Patient positioning is critical for accurate and precise scanning of the hip. The patient should be oriented with the long axis of the DXA table with appropriate hip abduction or adduction to align the femur shaft parallel to the long axis of the table (so that it will appear straight on the image). The foot positioner is useful to maintain the appropriate internal rotation of the femur. Without attention to proper femoral rotation and subsequent securing to the positioning device, it Volume 10, 2007
Standards and Guidelines for Central DXA is most likely that femoral internal rotation will be replaced by ankle inversion. Appropriate femoral rotation can best be achieved by holding the relaxed patient’s thigh and leg and internally rotating it. When scanning on a device that uses a hip sling to induce femoral rotation (i.e. Norland-Cooper Surgical), extreme care must be paid to insure that the thigh strap tension be applied consistently, and that any deviations from the manufacturers guidelines be recorded to insure identical degrees of rotation on follow-up exams. Appropriate positioning places the femoral neck parallel to the plane of the DXA table. The positioning laser is moved to a position 4 cm inferior to the greater trochanter or 1 cm inferior to the pubic symphysis in the midline of the thigh. During acquisition, ensure that the femur is straight and that the internal rotation of the femur is appropriate, as evidenced by a lack of prominence of the lesser trochanter. The greater trochanter should appear large and rounded, with soft tissue seen above the superior edge of the bone. There should be space between the femoral shaft and ischium.
Forearm Forearm scanning should be performed with the patient comfortably seated in a standard-height chair with no arms or wheels. The nondominant arm should be scanned, unless previously fractured. The forearm should be measured according to the manufacturer’s instructions, and its length entered. The elbow should be flexed between 90 and 105 . The laser should be positioned at a level that allows visualization of the first row of carpal bones proximally, therefore ensuring the inclusion of the 33% radius.
Scan Analysis General Although the specifics of DXA analysis are particular to each individual manufacturer (and detailed in the manufacturer’s manual), we now will discuss the parameters that are common to optimal DXA analysis, regardless of equipment type. Although software auto-analysis routines facilitate analysis, all automatically analyzed scans must be examined by the operator and verified to be correct or adjusted according to acceptable standard operating procedures. Features to watch for include properly placed regions of interest (ROIs), appropriate labeling of ROIs, complete bone maps (also called point typing or edge detection), and artifacts. The brightness and contrast features may help to facilitate these observations. If there has been correct patient positioning and scan acquisition, then scan analysis usually requires minimal operator intervention. Changes should be made if the auto-analysis obviously is incorrect, but operators should resist the temptation to ‘‘fiddle.’’ The compare or copy feature can be used to more precisely compare serial DXA scans, if they have been obtained with the same scan mode, software, and hardware. Positioning should be confirmed visually to be comparable between Journal of Clinical Densitometry
191 scans. The bone map mask from the baseline scan should be exactly superimposed on the bone map of the follow-up scan, with correspondence of bone mapping and ROIs.
Lumbar Spine Appropriate procedures for determining the validity of spine DXA scans include the following: Assessing each image for artifacts Excluding vertebral bodies with intrinsic or nonremovable overlying artifacts Ensuring that soft tissue radiodensities are not mapped as bone Taking note that the width of the ROI box need not be changed unless there has been a compression fracture. New vertebral fractures or surgery within the ROI can have a major impact on the interpretation of serial scans. In such cases, the initial scan must be reanalyzed and the level(s) affected must be excluded. Only then can the ‘‘compare’’ feature be used in the analysis of serial scans. Spinal angulation (scoliosis) makes it difficult to obtain consistent patient positioning, and this also may invalidate the ‘‘compare’’ feature. Although the software allows for angulation of the vertebral borders, operator intervention often is unnecessary for minimal scoliosis. Extreme scoliosis, especially when associated with rotation of the vertebral bodies or diffuse degenerative change, usually invalidates the spine measurement in its entirety. Proper assignment of vertebral levels (segmentation) within the vertebral ROI is extremely important. Incorrect or unusual patterns of segmentation can influence diagnostic categorization, and introduce very large errors in sequential scan precision. The effect of the overlying spinous and transverse processes of the vertebral posterior elements creates distinctive patterns, which can aid in the identification of vertebral levels. L5 has the appearance of a block letter ‘‘I’’ lying on its side; L4 is ‘‘X’’ or ‘‘H’’ shaped; and L3eL1 are ‘‘Y’’ or ‘‘U’’ shaped1. A line drawn across the top of the iliac crests will most closely transect the L4eL5 interspace. By convention, the technologist should label the vertebral bodies from the bottom-up, to ensure consistency between scans and to ensure that the normative databases used for comparison are relevant. Technologists should note that if a patient has six nonerib-bearing vertebrae due to a congenital absence of the 12th rib, and the operator counts from the last rib-bearing vertebra downward, T12 will be labeled incorrectly as L1. Consequently, L4 also will be mislabeled as L5, and the patient may be interpreted incorrectly as having low bone density. Obtaining previous spine radiographs to review spine levels can be helpful in difficult cases. Other vertebral abnormalities and their frequency in the normal population are well described. Other clues to the validity of the scan can be learned by observing the progression of bone mineral content (BMC) and area as one moves from L1 to L4. BMC increases from L1 to L2, further increases from L2 to L3, and either is the Volume 10, 2007
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Fig. 1. Manufacturer differences in femoral neck ROI placement (6).
same or less from L3 to L4. If this pattern is not seen, it is reasonable to examine carefully for artifacts or degenerative changes, which may provide justification to exclude one or more vertebral levels.
Hip Femoral analysis presents its own challenges. Appropriate procedures for analyzing hip DXA scans include the following: Assessing each image for artifacts
Completing the bone map, if required Verifying that each ROI is positioned according to the manufacturer’s instructions (Hologic only) Centering the femoral midline down the length of the femur and perpendicular to the femoral neck box. Recognizing that the ischium may need to be cut from the total hip ROI (‘‘neutralized’’). Note that the placement of the femoral neck ROI differs between equipment manufacturers. Failure to follow these instructions can invalidate the T-score and Z-score calculations (Fig. 1). One frequent error in hip analysis occurs when the software fails to correctly define the edge of the femoral head. Unless the bone map is corrected, this can produce incorrect placement of the femoral neck ROI and misalignment of the femoral neck axis (Fig. 2).
Forearm Forearm scanning has distinct manufacturer’s recommendations, as detailed in the equipment operating manuals. The distal end of the ulna should be visible at the top of the image. The boundaries of the overall and specific ROIs must be verified. The ultradistal ROI must exclude all cortical bone of the distal ulna and radius endplates. The 33% ROI should be fully visible and at the correct area of the forearm (7). The width of both the radius and ulna in the ROI should never be changed.
DXA Precision Assessment Fig. 2. Incorrect femoral neck ROI placement due to incorrect edge detection of the femoral head (arrow). After correct reanalysis, the femoral neck BMD increased by over 10% (from 0.918 g/cm2 to 1.015 g/cm2). Contributed by W. D. Leslie. Journal of Clinical Densitometry
Understanding the precision of a test (also called its reproducibility or repeatability) is essential to the interpretation of serial change. In bone densitometry, this is particularly important as the changes we seek to detect are small and frequently may fall within the precision error of the test. Precision in bone densitometry must be evaluated at each center and Volume 10, 2007
Standards and Guidelines for Central DXA with each DXA technologist, as it cannot be assumed that all technologists have equal skills. In addition to the importance of the scanning equipment’s performance, DXA precision is highly dependent on the technologist’s skill in positioning the patient and the analysis of the captured scan. Because precision is applied to a particular center’s patient population, precision assessment should be done on patients who are typical for that center. The manufacturer’s estimates of precision should not be used, as the manufacturer’s technologists may have different skills and its sampled population usually is young, is easy to position, and has normal bone density. Therefore, a manufacturer’s precision is an optimal value, not one that can be used in clinical practice. There is, as yet, no defined minimum precision standard. The ISCD position is to encourage precision assessment by each technologist after completion of at least 100 scans, and thereafter whenever their skills have changed or upon machine replacement or upgrade. A center should pool the precision estimates for all technologists to establish an estimate of site precision. Precision assessment is not research. It is an essential procedure for the operation of a DXA center. Verbal patient consent should be obtained before participation in precision assessment. Usually, it is not necessary to use a signed consent form, but this may vary according to local regulations and research ethics boards. The number of patients required to establish precision depends on statistical power calculations. As a minimum, precision assessment may be done by testing 15 patients in triplicate or 30 patients in duplicate for each skeletal site of interest. The patient should get off the table between tests that are conducted using standard positioning and analysis, in full accordance with the manufacturer’s recommendations. Same-day precision generally is better than different day precision (8); consequently, some groups recommend having the patient return for the repeat scan a few days after the first scan (9e10). Having the two scans performed by different technologists reflects clinical reality in most facilities. The ‘‘compare function’’ may be used when analyzing replicate scans. BMD values (g/cm2) from each skeletal site should be entered onto a spreadsheet to calculate the mean and root mean square standard deviation (RMS SD) for each set of replicates. These values then are summed and divided by the number of patients, and then the coefficient of variability (CV) and %CV calculated. Precision is best expressed as absolute g/cm2 rather than as a percentage value, as this avoids magnification of the precision error at lower bone densities. A Precision Calculator is available at www.iscd.org. From the precision estimate, the Least Significant Change (LSC 5 RMS SD 2.77) can be calculated as the smallest change in bone density at that skeletal site which can be detected with 95% confidence ( p 5 0.05). To determine if an observed change in BMD is statistically significant, the BMD values are subtracted and, if greater or equal to the LSC, the change should be reported as being statistically significant at a 95% level of confidence. Recently developed GE Lunar and Norland-Cooper Surgical software allows Journal of Clinical Densitometry
193 observers to test the validity of comparison scans when BMD in a given area of vertebra changes more than 2e3% between scans. A monitoring time interval (MTI), defined as the time required to achieve a significant change given an assumed rate of change in BMD for that patient and that skeletal site (MTI 5 LSC/anticipated rate of BMD change), can also be calculated.
Quality Assurance Procedures QA procedures need to be a standard procedure in DXA facilities, to control both for operator and machine variability. A DXA QA program is essential for the proper operation of a bone densitometry facility. QA consists of two distinct parts: Instrument Quality Control and Technologist Quality Control. Instrument QA is achieved by monitoring the machine’s performance over time. Technologist QA reflects reproducible positioning and analysis of patient scans. A precision study (discussed earlier in this article) will document how well a technologist can reproduce DXA scans. Instrument QA procedures should follow closely the manufacturer’s recommendations in the machine manual, as instrument calibration is dealt with differently by different manufacturers. GE and Norland instruments require an external calibration scan with a special phantom performed each day. Hologic machines internally calibrate, using a rotating internal calibration wheel or drum with each pixel measurement. Anthropometric phantom scanning is required for all systems. Scanning an anthropometric phantom tests both the machine parameters and the software features of edge detection and analysis. Such QA scanning will detect any machine calibration failure or drift over a period of time. This method of scanning also will detect changes resulting from maintenance and repair of the DXA machine. The phantom BMD, BMC, and area should be plotted on graphs based on Shewhart control charts. To construct a Shewhart chart, the anthropometric phantom is scanned 10 times without repositioning, and then a mean phantom BMD is calculated. The difference between this mean and the daily measured phantom BMD is plotted against time. A band is identified on the graph with lines at þ3 SD (or þ1.5%) and 3 SD (or 1.5%) from the mean, representing the upper and lower control limits. Hologic software maintains these charts automatically; Norland-Cooper Surgical maintains BMD charts only; and GE Lunar operators need to create and maintain these charts manually. The Shewhart charts are used to monitor phantom BMD, BMC, and area over time. Should the phantom BMD fall outside the upper and lower control limit band, the phantom must be rescanned immediately. If the rescan also falls outside the acceptable range, all further patient scans should be postponed until the machine has been serviced. If phantom BMD readings fall outside 1.5% of the mean, service should be scheduled as soon as possible. To detect longitudinal drift, Shewhart charts should be reviewed weekly. If BMC and area drift in Volume 10, 2007
194 the same direction, it may not be detectable by reviewing the BMD chart alone. A phantom log with all phantom scans should be maintained. Service logs should be maintained (including printouts of error messages) as should all service, government, and radiation survey reports. After any preventive maintenance (PM) or service, the phantom should be scanned 10 times without moving the phantom. If the mean BMD exceeds the mean of the daily phantom scans that were performed on the 10 d previous to the PM, the machine should be recalibrated, and a new mean established from a further 10 scans of the phantom. A 1% change in readings is considered within normal limits after any change in software.
Special Circumstances Sometimes, a patient referred for densitometry studies will present special challenges, not meeting the usual criteria and, thereby, requiring special consideration. Especially in these circumstances, close communication between the DXA technologist and the DXA clinician is essential to derive the most information from bone density testing. The densitometry technologist must be able to optimally adapt to special circumstances and perform studies in such patients, so as to obtain the best possible information. Special patient circumstances may require that the technologist choose patient-specific sites for study, due to artifacts, the patient exceeding the weight limit for the DXA scan table, the patient’s inability to lay flat, or underlying disease states such as hyperparathyroidism. When any of the above circumstances occur, measurement at the forearm is suggested. Artifacts may include bilateral hip replacement, spine surgery, degenerative changes, or severe scoliosis. Additionally, declining BMD due to primary hyperparathyroidism may be most significant at the forearm sites, though BMD at the radius typically does not increase with antiresorptive therapy. The World Health Organization’s diagnostic criteria for osteoporosis can be applied to forearm DXA results. Patients who are obese should be advised to hold their abdominal panniculus out of the ROI at the time of all assessments. Infrequently, pediatric DXA studies may be required. Such circumstances may include corticosteroid therapy, fragility fractures, and chronic illness. These studies are difficult to interpret for a variety of reasons: children have not achieved peak bone mass; their bone size (and hence bone area) is increasing; and current normative databases do not adjust for the pubertal stage. A diagnosis of osteoporosis in a child primarily must be based on clinical considerations, rather than solely on densitometry results. Pediatric studies must be performed using pediatric software and according to manufacturer-specific pediatric scanning protocols. Spine and total body are the preferred skeletal sites. Pediatric-sized positioning blocks for the spine may be required. Positioning for total body scans should Journal of Clinical Densitometry
Khan et al. strictly follow the manufacturer’s recommendations. The low/thin bone densityescanning mode may be required for younger children. If subsequent comparison scans are performed using standard mode, there will be great imprecision. Pediatric reference databases should be used to calculate Z-scores to compare the patient’s BMD with that of ageand sex-matched counterparts. If adjustments for bone age or pubertal status are made, these should be noted clearly and remarked upon in the report. Issues related to body size are particularly important in pediatric BMD testing, because many of the conditions that are the basis for testing also impair growth (11). Smaller skeletal size produces a lower area BMD (hence a lower age-matched Z-score) due to the inability of DXA to correct for unmeasured skeletal depth. At a minimum, an accurate height measurement should be obtained, with comparison to growth charts, to determine whether growth velocity is normal or impaired. Some groups also assess Z-scores in height-matched children (12). T-scores are meaningless in children, as children have not yet attained peak bone mass and the precision and LSC values calculated on adults may not be applicable due to the smaller areas and lower BMD found in children. Total body DXA may be useful in some special circumstances, and can include both BMD and analysis of body composition. Along with spine, total body DXA is a preferred site in children. Patients with eating disorders or after weightreduction surgeries may require total body studies. Total body DXA results are not recognized as diagnostic criteria for osteoporosis. Total body DXA appears to change slowly on osteoporosis therapies, making monitoring at this site problematic. If the scanning equipment at a site is replaced, the technologist is advised to do cross-calibration with the old equipment so that subsequent scans can be compared with the baseline of the old machinery.
Conclusions We encourage the adoption of standard procedures for the acquisition, analysis, and QA of DXA scans for Canadian patients. These guidelines will assist in the optimization of clinical practices, both in single-operator and in multi-operator facilities. By standardizing the technologic aspects of DXA, we hope to encourage higher quality DXA testing and consequently, improve care for patients with metabolic bone disease in Canada.
References 1. Khan AA, Brown J, Faulkner K, et al. 2002 Winter Standards and guidelines for performing central dual X-ray densitometry from the Canadian Panel of International Society for Clinical Densitometry. J Clin Densitom 5(4):435e445. 2. Khan AA, Bachrach L, Brown JP, et al. 2004 Standards and guidelines for performing central dual-energy x-ray absorptiometry in premenopausal women, men, and children. J Clin Densitom 7(1):51e64. 3. Kent GN, Price RI, Gutteridge DH, et al. 1990 Human lactation: forearm trabecular bone loss, increased bone turnover, and renal Volume 10, 2007
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4. 5. 6. 7.
conservation of calcium and inorganic phosphate with recovery of bone mass following weaning. J Bone Miner Res 5(4): 361e369. Sowers M, Corton G, Shapiro B, et al. 1993 Changes in bone density with lactation. JAMA 269(24):3130e3135. Karlsson C, Obrant KJ, Karlsson M. 2001 Pregnancy and lactation confer reversible bone loss in humans. Osteoporos Int 12(10):828e834. Watts NB. 2004 November Fundamentals and pitfalls of bone densitometry using dual-energy X-ray absorptiometry (DXA). Osteoporos Int 15(11):847e854. World Health Organization Study Group. Assessment of fracture risk and application to screening for postmenopausal osteoporosis. World Health Organization Technical Report Series. 1994; 843:1e129.
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195 8. El Hajj Fuleihan GE. 1995 Reproducibility of DXA densitometry: a model for bone loss estimates. J Bone Miner Res 10: 1004e1014. 9. Leslie WD. 2003 Fall Establishing a regional bone density program: lessons from the Manitoba experience. J Clin Densitom 6(3):275e282. 10. El Hajj Fuleihan GE. 2005 Summer Lebanese guidelines for osteoporosis assessment and treatment: who to test? What measures to use? When to treat? J Clin Densitom 8(2):148e163. 11. Leonard MB. 2005 Mar Assessment of bone mass following renal transplantation in Leonard MB. Assessment of bone mass following renal transplantation in children. Pediatr Nephrol 20(3):360e367. 12. Klaus G. 1998 Weight-/height-related bone mineral density is not reduced after renal transplantation. Pediatr Nephrol 12:343e348.
Volume 10, 2007
ISCD Canadian Standards
Standards and Guidelines for Technologists Performing Central Dual-Energy X-Ray Absorptiometry Aliya A. Khan,*,1 Anita Colquhoun,2 David A. Hanley,3 Lawrence G. Jankowski,4 Robert G. Josse,5 David L. Kendler,6 Brian Lentle,6 William D. Leslie,7 E. Michael Lewiecki,8 Elaine O’Neill,9 Stephen Robertson,10 Zeba A. Syed,11 S. Bobo Tanner,12 and Dave Webster13 1
Divisions of Endocrinology and Geriatrics, McMaster University, Hamilton, Ontario, Canada; 2Osteoporosis Program, Women’s College Hospital, Toronto, Ontario, Canada; 3Department of Medicine, University of Calgary, Calgary, Alberta, Canada; 4Illinois Bone and Joint Institute, Morton Grove, IL; 5St. Michael’s Osteoporosis Centre, University of Toronto, Toronto, Ontario, Canada; 6University of British Columbia, Vancouver, British Columbia, Canada; 7Departments of Medicine and Radiology, University of Manitoba, Manitoba, Canada; 8New Mexico Clinical Research & Osteoporosis Center, Albuquerque, NM; 9Halton Healthcare Services, Oakville Hospital, Halton, Ontario, Canada; 10Prohealth Clinical Research, Vancouver, British Columbia, Canada; 11Musculoskeletal Radiology, Hanover Hospital, Hanover, PA; 12 Divisions of Rheumatology and Allergy, Vanderbilt University, Nashville, TN; and 13Sudbury Regional Hospital, Sudbury, Ontario, Canada
Key Words: Bone density; osteoporosis; standards; technologist.
that a technologist adheres to essential elements of the bone density examination. As an important sequel to the Canadian Standards for physicians, this document details what technologists must do to produce quality bone densitometry results. The primary objectives of the ISCD are to promote education and ensure standardization of densitometry, so as to improve patient care for osteoporosis and metabolic bone disease. Each densitometry facility needs to develop its own guidelines to ensure optimal quality bone densitometry results. Although these guidelines may vary from one facility to the next, standard features common to all DXA testing are needed to ensure that appropriate information is supplied to referring physicians. In this document, we suggest standards for developing standard operating procedures, to be used in conjunction with the manufacturer’s recommendations for instrument maintenance and operation. In this paper, we will discuss all of the aspects of bone densitometry relevant to technologists, reviewing issues of relevance to all DXA manufacturers and not specific to individual technologies. These features include issues of quality
Introduction Standards of care from the Canadian Panel of the International Society for Clinical Densitometry (ISCD) have been developed to improve the quality of bone densitometry practice across Canada. This document follows Standards 1 and 2 previously published by the Canadian Panel (1,2). Optimizing technologist standards is a critical component of providing Canadians with high-quality bone density testing by dual-energy X-ray absorptiometry (DXA). Achieving high-precision bone mineral density (BMD) scans requires Received 11/08/06; Revised 01/10/07; Accepted 01/12/07. This document was created by the ISCD Canadian Regional Panel. The ISCD has approved this document as being relevant to local or regional needs and does not necessarily represent official ISCD positions or ISCD positions as they relate to this specific jurisdiction. *Address correspondence to: Aliya A. Khan, MD, FRCPC, FACP, Professor of Clinical Medicine, Divisions Endocrinology and Geriatrics, McMaster University, 209-331 Sheddon Avenue, Oakville, Ontario L6J 1X8, Canada. E-mail: [email protected]
189
190 assurance (QA), precision assessment, scan acquisition, scan analysis, and special circumstances. By applying standardized bone densitometry procedures, the quality of bone density scanning and patient care in Canada likely will improve greatly.
Scan Preparation and Setup Facilities need to adhere to a standardized approach to scanning to maintain diagnostic accuracy and reduce variability on serial scanning. As a general rule, technologists are advised to perform scans of at least two relevant skeletal sites. By doing so, if patients have features precluding analysis at any one site, a second valid site still is available for testing. Both the spine and hip should be scanned, whenever possible. If either site does not provide a valid result, then the forearm can be used as the second site. The contralateral (opposite) side should be scanned, if there is a history of previous fracture or surgery affecting the hip or forearm.
Patient Preparation for the Scan After having the patient remove footwear, an accurate height and weight must be obtained. For height measurement, hair should be flattened. Because height is such an important indicator of spinal compression fracture, stadiometric measurements should be used if possible. If a stadiometer is unavailable, a wall-mounted tape measure may be the next best option. Alternatively, a carpenter’s level on the horizontal arm of the scales measuring device will improve the precision of measurement on doctor’s office scales. The patient should be asked if there is a chance of pregnancy and, if pregnancy cannot be excluded, the scan must be delayed and the 10-d rule should be followed. Although recent pregnancy and breastfeeding are not contraindications to bone density testing, these produce transient, reversible changes in bone mass and therefore BMD testing ideally should be delayed for 6 mo postpartum (3e5). A scan also may need to be delayed if (1) a calcium supplement has been swallowed within 2 h, or (2) a radioactive isotope has been administered within 72 h (even longer when isotopes with long half-lives, such as iodine-131, indium-111, or gallium-67, have been used). Generally, in such circumstances, one should delay for 10e12 half-lives. A delay of 14 d is recommended if the patient has had a radiographic procedure involving contrast material. All metal overlying the scan area should be removed. If the metal on the clothing is not easily pushed aside, clothing should be removed and the patient gowned. (It often helps to ask each patient to wear a loose jogging suit to the densitometry session.) The patient then should lie comfortably on the scanning table, breathing normally. Patient biographical information must be entered carefully. Errors in this information will have important consequences, aside from misidentification of the patient. Sex assignment errors will affect the calculations of T-score and Z-score. Depending on the manufacturer, the patient’s race and weight also can affect both the T-score and Z-score. The ISCD Journal of Clinical Densitometry
Khan et al. recommends using a nonerace-adjusted (White) reference population database for all T-score calculations. Z-scores should be race-adjusted, where suitable reference data exist. For the purpose of Z-score calculations, the patient’s selfreported ethnicity should be used. Patient weight may affect the Z-score calculation when this software option is enabled, but the ISCD recommends against weight-adjusting the Z-score. The biography always should be updated on rescanning.
Scan Acquisition Scan mode may be chosen by machine default, but should be overridden by the operator if there are valid reasons to do so (e.g., body thickness requiring a slower scan speed). If, during the initial scanning, there is evidence of suboptimal positioning, the scanner should be stopped, the patient repositioned, and the scan restarted. Absolute attention to detail is critical in all aspects of patient positioning, scan acquisition, and analysis to ensure the highest quality densitometry, particularly for comparing serial scans. Proper technique will ensure that the best possible information is available for the reporting physician. BMD reports can significantly affect patient management, both in the initial determination of a patient’s fracture risk and in subsequent follow-up of patients on therapy.
Lumbar Spine The final preparation for a spine scan starts with the patient sitting at the center of the scan table aligned along the long axis of the table. Best positioning is achieved by guiding the patient with support to the supine position centered on the table. The appropriate positioning block must be chosen and placed under the patient’s legs to flatten the lumbar lordosis, according to the manufacturer’s instructions. Properly performed, this will permit easy segmentation of lumbar levels. The block size and orientation should be recorded and used for all follow-up evaluations with that same patient. Position the laser alignment beam 2 cm inferior to the umbilicus or 2 cm inferior to the xyphoid, depending on the manufacturer’s instructions. The scan should include at least part of L5, usually some of the iliac crest, and part of T12 with some rib. The spine must be aligned exactly with the long axis of the table and there must be equal soft tissue on each side of the spine. The presence of scoliosis will present major and often insurmountable problems for positioning.
Hip Patient positioning is critical for accurate and precise scanning of the hip. The patient should be oriented with the long axis of the DXA table with appropriate hip abduction or adduction to align the femur shaft parallel to the long axis of the table (so that it will appear straight on the image). The foot positioner is useful to maintain the appropriate internal rotation of the femur. Without attention to proper femoral rotation and subsequent securing to the positioning device, it Volume 10, 2007
Standards and Guidelines for Central DXA is most likely that femoral internal rotation will be replaced by ankle inversion. Appropriate femoral rotation can best be achieved by holding the relaxed patient’s thigh and leg and internally rotating it. When scanning on a device that uses a hip sling to induce femoral rotation (i.e. Norland-Cooper Surgical), extreme care must be paid to insure that the thigh strap tension be applied consistently, and that any deviations from the manufacturers guidelines be recorded to insure identical degrees of rotation on follow-up exams. Appropriate positioning places the femoral neck parallel to the plane of the DXA table. The positioning laser is moved to a position 4 cm inferior to the greater trochanter or 1 cm inferior to the pubic symphysis in the midline of the thigh. During acquisition, ensure that the femur is straight and that the internal rotation of the femur is appropriate, as evidenced by a lack of prominence of the lesser trochanter. The greater trochanter should appear large and rounded, with soft tissue seen above the superior edge of the bone. There should be space between the femoral shaft and ischium.
Forearm Forearm scanning should be performed with the patient comfortably seated in a standard-height chair with no arms or wheels. The nondominant arm should be scanned, unless previously fractured. The forearm should be measured according to the manufacturer’s instructions, and its length entered. The elbow should be flexed between 90 and 105 . The laser should be positioned at a level that allows visualization of the first row of carpal bones proximally, therefore ensuring the inclusion of the 33% radius.
Scan Analysis General Although the specifics of DXA analysis are particular to each individual manufacturer (and detailed in the manufacturer’s manual), we now will discuss the parameters that are common to optimal DXA analysis, regardless of equipment type. Although software auto-analysis routines facilitate analysis, all automatically analyzed scans must be examined by the operator and verified to be correct or adjusted according to acceptable standard operating procedures. Features to watch for include properly placed regions of interest (ROIs), appropriate labeling of ROIs, complete bone maps (also called point typing or edge detection), and artifacts. The brightness and contrast features may help to facilitate these observations. If there has been correct patient positioning and scan acquisition, then scan analysis usually requires minimal operator intervention. Changes should be made if the auto-analysis obviously is incorrect, but operators should resist the temptation to ‘‘fiddle.’’ The compare or copy feature can be used to more precisely compare serial DXA scans, if they have been obtained with the same scan mode, software, and hardware. Positioning should be confirmed visually to be comparable between Journal of Clinical Densitometry
191 scans. The bone map mask from the baseline scan should be exactly superimposed on the bone map of the follow-up scan, with correspondence of bone mapping and ROIs.
Lumbar Spine Appropriate procedures for determining the validity of spine DXA scans include the following: Assessing each image for artifacts Excluding vertebral bodies with intrinsic or nonremovable overlying artifacts Ensuring that soft tissue radiodensities are not mapped as bone Taking note that the width of the ROI box need not be changed unless there has been a compression fracture. New vertebral fractures or surgery within the ROI can have a major impact on the interpretation of serial scans. In such cases, the initial scan must be reanalyzed and the level(s) affected must be excluded. Only then can the ‘‘compare’’ feature be used in the analysis of serial scans. Spinal angulation (scoliosis) makes it difficult to obtain consistent patient positioning, and this also may invalidate the ‘‘compare’’ feature. Although the software allows for angulation of the vertebral borders, operator intervention often is unnecessary for minimal scoliosis. Extreme scoliosis, especially when associated with rotation of the vertebral bodies or diffuse degenerative change, usually invalidates the spine measurement in its entirety. Proper assignment of vertebral levels (segmentation) within the vertebral ROI is extremely important. Incorrect or unusual patterns of segmentation can influence diagnostic categorization, and introduce very large errors in sequential scan precision. The effect of the overlying spinous and transverse processes of the vertebral posterior elements creates distinctive patterns, which can aid in the identification of vertebral levels. L5 has the appearance of a block letter ‘‘I’’ lying on its side; L4 is ‘‘X’’ or ‘‘H’’ shaped; and L3eL1 are ‘‘Y’’ or ‘‘U’’ shaped1. A line drawn across the top of the iliac crests will most closely transect the L4eL5 interspace. By convention, the technologist should label the vertebral bodies from the bottom-up, to ensure consistency between scans and to ensure that the normative databases used for comparison are relevant. Technologists should note that if a patient has six nonerib-bearing vertebrae due to a congenital absence of the 12th rib, and the operator counts from the last rib-bearing vertebra downward, T12 will be labeled incorrectly as L1. Consequently, L4 also will be mislabeled as L5, and the patient may be interpreted incorrectly as having low bone density. Obtaining previous spine radiographs to review spine levels can be helpful in difficult cases. Other vertebral abnormalities and their frequency in the normal population are well described. Other clues to the validity of the scan can be learned by observing the progression of bone mineral content (BMC) and area as one moves from L1 to L4. BMC increases from L1 to L2, further increases from L2 to L3, and either is the Volume 10, 2007
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Fig. 1. Manufacturer differences in femoral neck ROI placement (6).
same or less from L3 to L4. If this pattern is not seen, it is reasonable to examine carefully for artifacts or degenerative changes, which may provide justification to exclude one or more vertebral levels.
Hip Femoral analysis presents its own challenges. Appropriate procedures for analyzing hip DXA scans include the following: Assessing each image for artifacts
Completing the bone map, if required Verifying that each ROI is positioned according to the manufacturer’s instructions (Hologic only) Centering the femoral midline down the length of the femur and perpendicular to the femoral neck box. Recognizing that the ischium may need to be cut from the total hip ROI (‘‘neutralized’’). Note that the placement of the femoral neck ROI differs between equipment manufacturers. Failure to follow these instructions can invalidate the T-score and Z-score calculations (Fig. 1). One frequent error in hip analysis occurs when the software fails to correctly define the edge of the femoral head. Unless the bone map is corrected, this can produce incorrect placement of the femoral neck ROI and misalignment of the femoral neck axis (Fig. 2).
Forearm Forearm scanning has distinct manufacturer’s recommendations, as detailed in the equipment operating manuals. The distal end of the ulna should be visible at the top of the image. The boundaries of the overall and specific ROIs must be verified. The ultradistal ROI must exclude all cortical bone of the distal ulna and radius endplates. The 33% ROI should be fully visible and at the correct area of the forearm (7). The width of both the radius and ulna in the ROI should never be changed.
DXA Precision Assessment Fig. 2. Incorrect femoral neck ROI placement due to incorrect edge detection of the femoral head (arrow). After correct reanalysis, the femoral neck BMD increased by over 10% (from 0.918 g/cm2 to 1.015 g/cm2). Contributed by W. D. Leslie. Journal of Clinical Densitometry
Understanding the precision of a test (also called its reproducibility or repeatability) is essential to the interpretation of serial change. In bone densitometry, this is particularly important as the changes we seek to detect are small and frequently may fall within the precision error of the test. Precision in bone densitometry must be evaluated at each center and Volume 10, 2007
Standards and Guidelines for Central DXA with each DXA technologist, as it cannot be assumed that all technologists have equal skills. In addition to the importance of the scanning equipment’s performance, DXA precision is highly dependent on the technologist’s skill in positioning the patient and the analysis of the captured scan. Because precision is applied to a particular center’s patient population, precision assessment should be done on patients who are typical for that center. The manufacturer’s estimates of precision should not be used, as the manufacturer’s technologists may have different skills and its sampled population usually is young, is easy to position, and has normal bone density. Therefore, a manufacturer’s precision is an optimal value, not one that can be used in clinical practice. There is, as yet, no defined minimum precision standard. The ISCD position is to encourage precision assessment by each technologist after completion of at least 100 scans, and thereafter whenever their skills have changed or upon machine replacement or upgrade. A center should pool the precision estimates for all technologists to establish an estimate of site precision. Precision assessment is not research. It is an essential procedure for the operation of a DXA center. Verbal patient consent should be obtained before participation in precision assessment. Usually, it is not necessary to use a signed consent form, but this may vary according to local regulations and research ethics boards. The number of patients required to establish precision depends on statistical power calculations. As a minimum, precision assessment may be done by testing 15 patients in triplicate or 30 patients in duplicate for each skeletal site of interest. The patient should get off the table between tests that are conducted using standard positioning and analysis, in full accordance with the manufacturer’s recommendations. Same-day precision generally is better than different day precision (8); consequently, some groups recommend having the patient return for the repeat scan a few days after the first scan (9e10). Having the two scans performed by different technologists reflects clinical reality in most facilities. The ‘‘compare function’’ may be used when analyzing replicate scans. BMD values (g/cm2) from each skeletal site should be entered onto a spreadsheet to calculate the mean and root mean square standard deviation (RMS SD) for each set of replicates. These values then are summed and divided by the number of patients, and then the coefficient of variability (CV) and %CV calculated. Precision is best expressed as absolute g/cm2 rather than as a percentage value, as this avoids magnification of the precision error at lower bone densities. A Precision Calculator is available at www.iscd.org. From the precision estimate, the Least Significant Change (LSC 5 RMS SD 2.77) can be calculated as the smallest change in bone density at that skeletal site which can be detected with 95% confidence ( p 5 0.05). To determine if an observed change in BMD is statistically significant, the BMD values are subtracted and, if greater or equal to the LSC, the change should be reported as being statistically significant at a 95% level of confidence. Recently developed GE Lunar and Norland-Cooper Surgical software allows Journal of Clinical Densitometry
193 observers to test the validity of comparison scans when BMD in a given area of vertebra changes more than 2e3% between scans. A monitoring time interval (MTI), defined as the time required to achieve a significant change given an assumed rate of change in BMD for that patient and that skeletal site (MTI 5 LSC/anticipated rate of BMD change), can also be calculated.
Quality Assurance Procedures QA procedures need to be a standard procedure in DXA facilities, to control both for operator and machine variability. A DXA QA program is essential for the proper operation of a bone densitometry facility. QA consists of two distinct parts: Instrument Quality Control and Technologist Quality Control. Instrument QA is achieved by monitoring the machine’s performance over time. Technologist QA reflects reproducible positioning and analysis of patient scans. A precision study (discussed earlier in this article) will document how well a technologist can reproduce DXA scans. Instrument QA procedures should follow closely the manufacturer’s recommendations in the machine manual, as instrument calibration is dealt with differently by different manufacturers. GE and Norland instruments require an external calibration scan with a special phantom performed each day. Hologic machines internally calibrate, using a rotating internal calibration wheel or drum with each pixel measurement. Anthropometric phantom scanning is required for all systems. Scanning an anthropometric phantom tests both the machine parameters and the software features of edge detection and analysis. Such QA scanning will detect any machine calibration failure or drift over a period of time. This method of scanning also will detect changes resulting from maintenance and repair of the DXA machine. The phantom BMD, BMC, and area should be plotted on graphs based on Shewhart control charts. To construct a Shewhart chart, the anthropometric phantom is scanned 10 times without repositioning, and then a mean phantom BMD is calculated. The difference between this mean and the daily measured phantom BMD is plotted against time. A band is identified on the graph with lines at þ3 SD (or þ1.5%) and 3 SD (or 1.5%) from the mean, representing the upper and lower control limits. Hologic software maintains these charts automatically; Norland-Cooper Surgical maintains BMD charts only; and GE Lunar operators need to create and maintain these charts manually. The Shewhart charts are used to monitor phantom BMD, BMC, and area over time. Should the phantom BMD fall outside the upper and lower control limit band, the phantom must be rescanned immediately. If the rescan also falls outside the acceptable range, all further patient scans should be postponed until the machine has been serviced. If phantom BMD readings fall outside 1.5% of the mean, service should be scheduled as soon as possible. To detect longitudinal drift, Shewhart charts should be reviewed weekly. If BMC and area drift in Volume 10, 2007
194 the same direction, it may not be detectable by reviewing the BMD chart alone. A phantom log with all phantom scans should be maintained. Service logs should be maintained (including printouts of error messages) as should all service, government, and radiation survey reports. After any preventive maintenance (PM) or service, the phantom should be scanned 10 times without moving the phantom. If the mean BMD exceeds the mean of the daily phantom scans that were performed on the 10 d previous to the PM, the machine should be recalibrated, and a new mean established from a further 10 scans of the phantom. A 1% change in readings is considered within normal limits after any change in software.
Special Circumstances Sometimes, a patient referred for densitometry studies will present special challenges, not meeting the usual criteria and, thereby, requiring special consideration. Especially in these circumstances, close communication between the DXA technologist and the DXA clinician is essential to derive the most information from bone density testing. The densitometry technologist must be able to optimally adapt to special circumstances and perform studies in such patients, so as to obtain the best possible information. Special patient circumstances may require that the technologist choose patient-specific sites for study, due to artifacts, the patient exceeding the weight limit for the DXA scan table, the patient’s inability to lay flat, or underlying disease states such as hyperparathyroidism. When any of the above circumstances occur, measurement at the forearm is suggested. Artifacts may include bilateral hip replacement, spine surgery, degenerative changes, or severe scoliosis. Additionally, declining BMD due to primary hyperparathyroidism may be most significant at the forearm sites, though BMD at the radius typically does not increase with antiresorptive therapy. The World Health Organization’s diagnostic criteria for osteoporosis can be applied to forearm DXA results. Patients who are obese should be advised to hold their abdominal panniculus out of the ROI at the time of all assessments. Infrequently, pediatric DXA studies may be required. Such circumstances may include corticosteroid therapy, fragility fractures, and chronic illness. These studies are difficult to interpret for a variety of reasons: children have not achieved peak bone mass; their bone size (and hence bone area) is increasing; and current normative databases do not adjust for the pubertal stage. A diagnosis of osteoporosis in a child primarily must be based on clinical considerations, rather than solely on densitometry results. Pediatric studies must be performed using pediatric software and according to manufacturer-specific pediatric scanning protocols. Spine and total body are the preferred skeletal sites. Pediatric-sized positioning blocks for the spine may be required. Positioning for total body scans should Journal of Clinical Densitometry
Khan et al. strictly follow the manufacturer’s recommendations. The low/thin bone densityescanning mode may be required for younger children. If subsequent comparison scans are performed using standard mode, there will be great imprecision. Pediatric reference databases should be used to calculate Z-scores to compare the patient’s BMD with that of ageand sex-matched counterparts. If adjustments for bone age or pubertal status are made, these should be noted clearly and remarked upon in the report. Issues related to body size are particularly important in pediatric BMD testing, because many of the conditions that are the basis for testing also impair growth (11). Smaller skeletal size produces a lower area BMD (hence a lower age-matched Z-score) due to the inability of DXA to correct for unmeasured skeletal depth. At a minimum, an accurate height measurement should be obtained, with comparison to growth charts, to determine whether growth velocity is normal or impaired. Some groups also assess Z-scores in height-matched children (12). T-scores are meaningless in children, as children have not yet attained peak bone mass and the precision and LSC values calculated on adults may not be applicable due to the smaller areas and lower BMD found in children. Total body DXA may be useful in some special circumstances, and can include both BMD and analysis of body composition. Along with spine, total body DXA is a preferred site in children. Patients with eating disorders or after weightreduction surgeries may require total body studies. Total body DXA results are not recognized as diagnostic criteria for osteoporosis. Total body DXA appears to change slowly on osteoporosis therapies, making monitoring at this site problematic. If the scanning equipment at a site is replaced, the technologist is advised to do cross-calibration with the old equipment so that subsequent scans can be compared with the baseline of the old machinery.
Conclusions We encourage the adoption of standard procedures for the acquisition, analysis, and QA of DXA scans for Canadian patients. These guidelines will assist in the optimization of clinical practices, both in single-operator and in multi-operator facilities. By standardizing the technologic aspects of DXA, we hope to encourage higher quality DXA testing and consequently, improve care for patients with metabolic bone disease in Canada.
References 1. Khan AA, Brown J, Faulkner K, et al. 2002 Winter Standards and guidelines for performing central dual X-ray densitometry from the Canadian Panel of International Society for Clinical Densitometry. J Clin Densitom 5(4):435e445. 2. Khan AA, Bachrach L, Brown JP, et al. 2004 Standards and guidelines for performing central dual-energy x-ray absorptiometry in premenopausal women, men, and children. J Clin Densitom 7(1):51e64. 3. Kent GN, Price RI, Gutteridge DH, et al. 1990 Human lactation: forearm trabecular bone loss, increased bone turnover, and renal Volume 10, 2007
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conservation of calcium and inorganic phosphate with recovery of bone mass following weaning. J Bone Miner Res 5(4): 361e369. Sowers M, Corton G, Shapiro B, et al. 1993 Changes in bone density with lactation. JAMA 269(24):3130e3135. Karlsson C, Obrant KJ, Karlsson M. 2001 Pregnancy and lactation confer reversible bone loss in humans. Osteoporos Int 12(10):828e834. Watts NB. 2004 November Fundamentals and pitfalls of bone densitometry using dual-energy X-ray absorptiometry (DXA). Osteoporos Int 15(11):847e854. World Health Organization Study Group. Assessment of fracture risk and application to screening for postmenopausal osteoporosis. World Health Organization Technical Report Series. 1994; 843:1e129.
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195 8. El Hajj Fuleihan GE. 1995 Reproducibility of DXA densitometry: a model for bone loss estimates. J Bone Miner Res 10: 1004e1014. 9. Leslie WD. 2003 Fall Establishing a regional bone density program: lessons from the Manitoba experience. J Clin Densitom 6(3):275e282. 10. El Hajj Fuleihan GE. 2005 Summer Lebanese guidelines for osteoporosis assessment and treatment: who to test? What measures to use? When to treat? J Clin Densitom 8(2):148e163. 11. Leonard MB. 2005 Mar Assessment of bone mass following renal transplantation in Leonard MB. Assessment of bone mass following renal transplantation in children. Pediatr Nephrol 20(3):360e367. 12. Klaus G. 1998 Weight-/height-related bone mineral density is not reduced after renal transplantation. Pediatr Nephrol 12:343e348.
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