Low energy availability surrogates associated with lower bone mineral density and bone stress injury site
Abstract
Background: Exercise is an osteogenic stimulus that should increase bone mineral density (BMD) and protect against injury. However, some female athletes have lower BMD and increased bone stress injury (BSI) risk. Impaired bone health seen in athletes may be explained by low energy availability as described by concepts of Relative Energy Deficiency in Sport (RED‐S) and Female Athlete Triad (Triad). Objective: To elucidate the relationship between RED‐S/Triad risk factors and BSI to high‐risk (femoral neck, sacrum) and low‐risk (other) bones. Design: Cross‐sectional survey and retrospective chart review. Setting: Tertiary care academic center. Patients: Female athletes aged 15–30 years participating in ≥4 h/week of exercise presenting to sports medicine/orthopedics clinic who had a self‐reported BSI and available dual‐energy x‐ray absorptiometry (DXA) measurement of BMD. Interventions: Not applicable. Main Outcome Measurements: Location of BSI. Results: In 127 athletes, high‐risk BSI was associated with surrogates of low energy availability ( p = .032) and having a DXA Z‐score < −1 ( p = .035) but not a current/past history of menstrual dysfunction ( p = .348). Accumulating RED‐S/Triad risk factors increase the odds of incurring a high‐risk BSI ( p = .048). Conclusions: Adolescent/young female athletes who sustain BSI at high‐risk sites (femoral neck, sacrum) may have underlying risk factors (eg, low energy availability, poor overall bone health) that should prompt further workup and referral to optimize health in these athletes.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Holtzman et al. found 20/28 (71.4%) athletes with a history of high-risk stress injuries had LEA (p = 0.032).
“Holtzman et al. [86] Female athletes ages 15-30 (n = 127) 20/28 (71.4%) athletes with a history of high-risk stress injuries (affecting the sacrum, pelvis, or femoral neck) had LEA (p = 0.032).”
From Low Energy Availability and Relative Energy Deficiency in Sport: A Systematic Review and Meta-analysis (2025) · cites this paper as [86]
Holtzman et al. found 48/99 (48.5%) athletes with a history of low-risk stress injuries had LEA (p = 0.032).
“48/99 (48.5%) athletes with a history of low-risk stress injuries (not affecting the sacrum, pelvis, or femoral neck) had LEA (p = 0.032).”
From Low Energy Availability and Relative Energy Deficiency in Sport: A Systematic Review and Meta-analysis (2025) · cites this paper as [86]
Cites
1 retracted
Retracted: Prevalence and factors associated with bone stress injury in middle school runners
Tenforde, A. S., DeLuca, S., Wu, A. C., Ackerman, K. E., Lewis, M., Rauh, M. J., Heiderscheit, B. C., Krabak, B. J., Kraus, E., Roberts, W. O., et al. (2021) · PM&R · doi:10.1002/pmrj.12673 · Cited by 33 · see citing works
Self-citationRetractedRADIOGRAPHIC ATLAS OF SKELETAL DEVELOPMENT OF THE HAND AND WRIST
GREULICH, W. W., & Pyle, S. I. (1959) · The American Journal of the Medical Sciences · doi:10.1097/00000441-195909000-00030 · Cited by 5,598 · see citing works
American College of Sports Medicine position stand
Otis, C. L. (1997) · Medical Entomology and Zoology · Cited by 4,407 · see citing works
(2007) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e318149f111 · Cited by 1,554 · see citing works
Mountjoy, M., Sundgot-Borgen, J., Burke, L., Carter, S., Constantini, N., Lebrun, C., Meyer, N., Sherman, R., Steffen, K., Budgett, R., et al. (2014) · British Journal of Sports Medicine · doi:10.1136/bjsports-2014-093502 · Cited by 1,469 · cited 9× · see citing works
“Although only one of these surrogates—selfreported eating habits—is in line with Marx and colleagues(18) and Nattiv and colleagues,(19) our surrogates correlate well with established negative sequelae of inadequate EA, such as endocrine and metabolic dysfunction, psychological disruptions, and decreased response to tr…”
BackgroundInfluentialPhysical Activity and Bone Health
Kohrt, W. M., Bloomfield, S. A., Little, K. D., Nelson, M. E., & Yingling, V. R. (2004) · Medicine & Science in Sports & Exercise · doi:10.1249/01.mss.0000142662.21767.58 · Cited by 1,043 · see citing works
Bailey, D. A., McKay, H. A., Mirwald, R. L., Crocker, P. R. E., & Faulkner, R. A. (1999) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.1999.14.10.1672 · Cited by 1,032 · see citing works
IOC consensus statement on relative energy deficiency in sport (RED-S): 2018 update
Mountjoy, M., Sundgot-Borgen, J. K., Burke, L. M., Ackerman, K. E., Blauwet, C., Constantini, N., Lebrun, C., Lundy, B., Melin, A. K., Meyer, N. L., et al. (2018) · British Journal of Sports Medicine · doi:10.1136/bjsports-2018-099193 · Cited by 883 · see citing works
Self-citationLoucks, A. B., & Thuma, J. R. (2003) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-020369 · Cited by 760 · see citing works
De Souza, M. J., Nattiv, A., Joy, E., Misra, M., Williams, N. I., Mallinson, R. J., Gibbs, J. C., Olmsted, M., Goolsby, M., Matheson, G., et al. (2014) · British Journal of Sports Medicine · doi:10.1136/bjsports-2013-093218 · Cited by 661 · see citing works
Shuhart, C., Yeap, S. S., Anderson, P. A., Jankowski, L. G., Lewiecki, E. M., Morse, L. R., Rosen, H. N., Weber, D. R., Zemel, B. S., & Shepherd, J. (2019) · Journal of Clinical Densitometry · doi:10.1016/j.jocd.2019.07.001 · Cited by 538 · see citing works
Dose-Response Relationships Between Energy Availability and Bone Turnover in Young Exercising Women
Ihle, R., & Loucks, A. B. (2004) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.040410 · Cited by 523 · see citing works
Melin, A., Tornberg, Å. B., Skouby, S., Faber, J., Ritz, C., Sjödin, A., & Sundgot-Borgen, J. (2014) · British Journal of Sports Medicine · doi:10.1136/bjsports-2013-093240 · Cited by 435 · see citing works
The contribution of bone loss to postmenopausal osteoporosis
Hui, S. L., Slemenda, C. W., & Johnston, C. C. (1990) · Osteoporosis International · doi:10.1007/bf01880413 · Cited by 421 · see citing works
Pathophysiology of Age-Related Bone Loss and Osteoporosis
Khosla, S., & Riggs, B. L. (2005) · Endocrinology and Metabolism Clinics of North America · doi:10.1016/j.ecl.2005.07.009 · Cited by 376 · see citing works
Barrack, M. T., Gibbs, J. C., De Souza, M. J., Williams, N. I., Nichols, J. F., Rauh, M. J., & Nattiv, A. (2014) · The American Journal of Sports Medicine · doi:10.1177/0363546513520295 · Cited by 349 · see citing works
Energy balance and body composition in sports and exercise
Loucks, A. B. (2004) · Journal of Sports Sciences · doi:10.1080/0264041031000140518 · Cited by 344 · see citing works
Correlation of MRI Grading of Bone Stress Injuries With Clinical Risk Factors and Return to Play
Nattiv, A., Kennedy, G., Barrack, M. T., Abdelkerim, A., Goolsby, M. A., Arends, J. C., & Seeger, L. L. (2013) · The American Journal of Sports Medicine · doi:10.1177/0363546513490645 · Cited by 285 · see citing works
Wentz, L. M., Liu, P.-Y., Haymes, E., & Ilich, J. (2011) · Military Medicine · doi:10.7205/milmed-d-10-00322 · Cited by 260 · see citing works
Four simple questions can help screen for eating disorders
Cotton, M.-A., Ball, C., & Robinson, P. H. (2003) · Journal of General Internal Medicine · doi:10.1046/j.1525-1497.2003.20374.x · Cited by 260 · see citing works
Torstveit, M. K., & Sundgot-Borgen, J. (2005) · British Journal of Sports Medicine · doi:10.1136/bjsm.2003.011338 · Cited by 250 · see citing works
Ackerman, K. E., Holtzman, B., Cooper, K. M., Flynn, E. F., Bruinvels, G., Tenforde, A. S., Popp, K. L., Simpkin, A. J., & Parziale, A. L. (2019) · British Journal of Sports Medicine · doi:10.1136/bjsports-2017-098958 · Cited by 245 · see citing works
Self-citationTenforde, A. S., Carlson, J. L., Chang, A. O., Sainani, K. L., Shultz, R., Kim, J. H., Cutti, P., Golden, N. H., & Fredericson, M. (2016) · The American Journal of Sports Medicine · doi:10.1177/0363546516676262 · Cited by 230 · see citing works
Self-citationEndocrine Effects of Relative Energy Deficiency in Sport
Elliott-Sale, K. J., Tenforde, A. S., Parziale, A. L., Holtzman, B., & Ackerman, K. E. (2018) · International Journal of Sport Nutrition and Exercise Metabolism · doi:10.1123/ijsnem.2018-0127 · Cited by 229 · see citing works
Self-citationStress Fractures of the Femoral Neck
Egol, K. A., Koval, K. J., Kummer, F. J., & Frankel, V. H. (1998) · Clinical Orthopaedics and Related Research · doi:10.1097/00003086-199803000-00013 · Cited by 221 · see citing works
Identifying Sex-Specific Risk Factors for Stress Fractures in Adolescent Runners
Tenforde, A. S., Sayres, L. C., McCurdy, M. L., Sainani, K. L., & Fredericson, M. (2013) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0b013e3182963d75 · Cited by 197 · see citing works
Self-citationFractures in Relation to Menstrual Status and Bone Parameters in Young Athletes
Ackerman, K. E., Sokoloff, N. C., Maffazioli, G. D. N., Clarke, H., Lee, H., & Misra, M. (2014) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000000574 · Cited by 179 · see citing works
Self-citationStress fractures: diagnosis, treatment, and prevention.
Patel, D. S., Roth, M., & Kapil, N. (2011) · PubMed · Cited by 152 · see citing works
The Development of the Brief Eating Disorder in Athletes Questionnaire
Martinsen, M., Holme, I., Pensgaard, A. M., Torstveit, M. K., & Sundgot-Borgen, J. K. (2014) · Medicine & Science in Sports & Exercise · doi:10.1249/mss.0000000000000276 · Cited by 136 · see citing works
High‐Risk Stress Fractures: Diagnosis and Management
McInnis, K. C., & Ramey, L. N. (2016) · PM&R · doi:10.1016/j.pmrj.2015.09.019 · Cited by 135 · see citing works
Reduced energy availability: implications for bone health in physically active populations
Papageorgiou, M., Dolan, E., Elliott-Sale, K., & Sale, C. (2017) · European Journal of Nutrition · doi:10.1007/s00394-017-1498-8 · Cited by 125 · see citing works
Stress Fracture Sites Related to Underlying Bone Health in Athletic Females
Marx, R. G., Saint‐Phard, D., Callahan, L. R., Chu, J., & Hannafin, J. A. (2001) · Clinical Journal of Sport Medicine · doi:10.1097/00042752-200104000-00002 · Cited by 94 · see citing works
The Bone Metabolic Response to Exercise and Nutrition
Dolan, E., Varley, I., Ackerman, K. E., Pereira, R. M. R., Elliott-Sale, K. J., & Sale, C. (2019) · Exercise and Sport Sciences Reviews · doi:10.1249/jes.0000000000000215 · Cited by 94 · see citing works
Self-citationTenforde, A. S., Parziale, A. L., Popp, K. L., & Ackerman, K. E. (2017) · The American Journal of Sports Medicine · doi:10.1177/0363546517730584 · Cited by 82 · see citing works
Self-citationHoenig, T., Tenforde, A. S., Strahl, A., Rolvien, T., & Hollander, K. (2021) · The American Journal of Sports Medicine · doi:10.1177/0363546521993807 · Cited by 67 · see citing works
Self-citationSouthmayd, E. A., Mallinson, R. J., Williams, N. I., Mallinson, D. J., & Souza, M. D. D. (2017) · Osteoporosis International · doi:10.1007/s00198-016-3887-x · Cited by 63 · see citing works
Relative Energy Deficiency in Sport (RED-S)
(2015) · British Journal of Sports Medicine · doi:10.1136/bjsports-2014-094559 · Cited by 59 · see citing works
Stress fractures of the femoral neck in runners: a review
Neubauer, T., Brand, J., Lidder, S., & Krawany, M. (2016) · Research in Sports Medicine · doi:10.1080/15438627.2016.1191489 · Cited by 48 · see citing works
Displaced stress fracture of the femoral neck in young active adults
Polacek, M., & Småbrekke, A. (2010) · BMJ Case Reports · doi:10.1136/bcr.02.2010.2749 · Cited by 25 · see citing works
Henning, P. T. (2014) · Sports Health A Multidisciplinary Approach · doi:10.1177/1941738114523381 · Cited by 19 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Mountjoy, M., Ackerman, K. E., Bailey, D. M., Burke, L. M., Constantini, N., Hackney, A. C., Heikura, I. A., Melin, A., Pensgaard, A. M., Stellingwerff, T., et al. (2023) · British Journal of Sports Medicine · doi:10.1136/bjsports-2023-106994 · Cited by 724 · see citing works
Self-citationStellingwerff, T., Mountjoy, M., McCluskey, W. T., Ackerman, K. E., Verhagen, E., & Heikura, I. A. (2023) · British Journal of Sports Medicine · doi:10.1136/bjsports-2023-106914 · Cited by 119 · see citing works
Self-citationGallant, T. L., Ong, L. F., Wong, L., Sparks, M., Wilson, E., Puglisi, J. L., & Gerriets, V. A. (2025) · Sports Medicine · doi:10.1007/s40279-024-02130-0 · Cited by 75 · see citing works
Bonilla, D. A., Cardozo, L. A., Vélez-Gutiérrez, J. M., Arévalo-Rodríguez, A., Vargas-Molina, S., Stout, J. R., Kreider, R. B., & Petro, J. L. (2022) · International Journal of Environmental Research and Public Health · doi:10.3390/ijerph191912710 · Cited by 73 · see citing works
From Tissue to System: What Constitutes an Appropriate Response to Loading?
Gabbett, T. J., & Oetter, E. (2024) · Sports Medicine · doi:10.1007/s40279-024-02126-w · Cited by 48 · see citing works
Ackerman, K. E., Rogers, M. A., Heikura, I. A., Burke, L. M., Stellingwerff, T., Hackney, A. C., Verhagen, E., Schley, S., Saville, G. H., Mountjoy, M., et al. (2023) · British Journal of Sports Medicine · doi:10.1136/bjsports-2023-107359 · Cited by 43 · see citing works
Self-citationSchulz, J. M., Pohlod, L., Myers, S., Chung, J., & Thornton, J. S. (2024) · Journal of sport and health science/Journal of Sport and Health Science · doi:10.1016/j.jshs.2024.100981 · Cited by 31 · see citing works
Heikura, I. A., McCluskey, W. T. P., Tsai, M., Johnson, L. J., Murray, H. J., Mountjoy, M. L., Ackerman, K. E., Fliss, M. D., & Stellingwerff, T. (2024) · British Journal of Sports Medicine · doi:10.1136/bjsports-2024-108121 · Cited by 29 · see citing works
Self-citationSouza, M. D. D., Williams, N., Misra, M., Nattiv, A., Joy, E. A., Barrack, M., Ricker, E. A., Gorrell, S., Koltun, K. J., O'Donnell, E., et al. (2025) · Sports Medicine · doi:10.1007/s40279-025-02333-z · Cited by 21 · see citing works
von Brackel, F. N., Munzinger, R., Bartosik, M., Simon, A., Barvencik, F., Oheim, R., & Amling, M. (2025) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.70082 · Cited by 14 · see citing works
Tenforde, A. S., Ackerman, K. E., Bouxsein, M., Gaudette, L. W., McCall, L. M., Rudolph, S., Gehman, S., Garrahan, M., Hughes, J. M., Outerleys, J. B., et al. (2024) · Orthopaedic Journal of Sports Medicine · doi:10.1177/23259671241246227 · Cited by 11 · see citing works
Self-citationStürznickel, J., Hinz, N., Delsmann, M. M., Hoenig, T., & Rolvien, T. (2022) · The American Journal of Sports Medicine · doi:10.1177/03635465221120385 · Cited by 10 · see citing works
Koivisto, A., Steffen, K., Finnes, T. E., Pretorius, M., & Berge, H. M. (2023) · Frontiers in Sports and Active Living · doi:10.3389/fspor.2023.1246828 · Cited by 6 · see citing works
Hormonal contraception for female athletes presents special needs and concerns
Seidman, L., Seidman, D. S., & Constantini, N. (2023) · The European Journal of Contraception & Reproductive Health Care · doi:10.1080/13625187.2023.2287960 · Cited by 5 · see citing works
Low Energy Availability and Its Impact on Bone Health and Metabolism in Athletes: A Narrative Review
Konvička, J., Káňová, M., Borzenko, M., Petřeková, K., & Bužga, M. (2025) · Physiological Research · doi:10.33549/physiolres.935749 · Cited by 4 · see citing works
Gaudette, L. W., Ackerman, K. E., Bouxsein, M., Bruneau, M. M., Júnior, J. R. D. S., Garrahan, M., Gehman, S., Hughes, J. M., Outerleys, J. B., Willy, R. W., et al. (2025) · BMJ Open Sport & Exercise Medicine · doi:10.1136/bmjsem-2025-002469 · Cited by 2 · see citing works
Self-citationStellingwerff, T., Tsai, M., McCluskey, W. T. P., Burke, L. M., Fliss, M. D., Ackerman, K. E., & Heikura, I. A. (2026) · Sports Medicine · doi:10.1007/s40279-026-02478-5 · Cited by 2 · see citing works
Self-citationInfluence of professional sports activities on bone mineral density (literature review)
Игоревна, Н. К., Vykhodets, I. Т., Абрамова, Т. Ф., & Михайловна, Н. Т. (2024) · Russian Osteopathic Journal · doi:10.32885/2220-0975-2024-1-106-117 · Cited by 1 · see citing works
Spinello, G., Grigoletto, D., Cerea, S., Casali, N., Ghisi, M., Marcolin, G., Paoli, A., & Moro, T. (2026) · BMC Sports Science Medicine and Rehabilitation · doi:10.1186/s13102-026-01639-3 · Cited by 1 · see citing works
Impact of relative energy deficiency in sport on adolescent athletes
Catalan, M.-A., & Wiener, S. (2026) · Current Opinion in Pediatrics · doi:10.1097/mop.0000000000001578 · Cited by 1 · see citing works
Female athlete triad (fat): identifikasi risiko pada atlet putri papua
Sinaga, E., Putra, M. F. P., & Sinaga, E. (2023) · Multilateral Jurnal Pendidikan Jasmani dan Olahraga · doi:10.20527/multilateral.v22i4.16795
Die Frau im Sport – was ist anders?
Wieloch, N., & Scherr, J. (2025) · Sportphysio · doi:10.1055/a-2468-4423
Frauen im Sport – Geschlechtsspezifische Unterschiede
Wieloch, N., & Scherr, J. (2025) · physiopraxis · doi:10.1055/a-2561-7297
Vendlinski, S. S., Gorrell, S., Downey, A. E., Mehta, A. S., Grange, D. L., Machen, V. I., Accurso, E. C., Buckelew, S. M., Kapphahn, C., Moscicki, B. A., et al. (2025) · International Journal of Eating Disorders · doi:10.1002/eat.24569
Steinberg, N., Elbaz, L., Eliakim, A., Nemet, D., & Dar, G. (2026) · Physical Therapy in Sport · doi:10.1016/j.ptsp.2026.101888
Fitch, A. S., Mara, J. K., Lord, F., & Waddington, G. S. (2026) · Sports Medicine · doi:10.1007/s40279-026-02416-5
Comprehensive overview of bone disease in oncology patients
Špániková, B. (2026) · Clinical Osteology · doi:10.36290/clo.2026.004
Svoboda, J., & Hřivnová, M. (2026) · Hygiena · doi:10.21101/hygiena.a1912
Grønhaug, G., Slagel, N., & Sæterbakken, A. H. (2026) · Frontiers in Sports and Active Living · doi:10.3389/fspor.2026.1886526 · Cited by 1 · see citing works
The Unique Features of Pediatric Sports Injuries: The Hip
Henry, L. E., Funk, K., Yen, Y., & Abzug, J. M. (2026) · Children · doi:10.3390/children13091229
- Authors
- Holtzman, B., Popp, K. L., Tenforde, A. S., Parziale, A. L., Taylor, K., & Ackerman, K. E.
- Affiliations
- Boston Children's Hospital (US)
- U.S. Army Research Institute of Environmental Medicine (US)
- Corresponding author
- Ackerman, Kathryn E.
- Venue
- PM&R
- Publisher
- Wiley
- Published
- 2022-05
- Volume
- 14
- Issue
- 5
- Pages
- 587-596
- ISSN
- 1934-1482 (ISSN-L)
- 1934-1563
- OpenAlex
- W4224313850
- Cited by
- 30
- References
- 40
- Citations by year
- 2026: 9 · 2025: 7 · 2024: 6 · 2023: 6 · 2022: 2
- FWCI
- 1.53
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- PM&R (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Physical Sciences › Engineering › Biomedical Engineering › Lower Extremity Biomechanics and Pathologies
- Health Sciences › Medicine › Orthopedics and Sports Medicine › Bone health and osteoporosis research
- Social Sciences › Psychology › Clinical Psychology › Eating Disorders and Behaviors
- Keywords
- bone stress injuries, low energy availability, relative energy deficiency in sport, female athlete triad, bone mineral density, female athletes, femoral neck, sacrum, menstrual disorders, youth athletes
- MeSH terms
- Adolescent, Cross-Sectional Studies, Female, Humans, Retrospective Studies, Absorptiometry, Photon, Bone Density, Female Athlete Triad Syndrome, Athletes
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review