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June 23, 1993, Vol 269, No. 24 >
ARTICLE | June 23, 1993

Changes in Bone Density With Lactation FREE

MaryFran Sowers, PhD; Genie Corton; Brahm Shapiro, MD; Mary L. Jannausch, MS; Mary Crutchfield; Mindy L. Smith, MD; John F. Randolph, MD; Bruce Hollis, PhD
[+] Author Affiliations

Reprint requests to Department of Epidemiology, University of Michigan, 109 Observatory St, Ann Arbor, MI 48109-2029 (Dr Sowers).


JAMA. 1993;269(24):3130-3135. doi:10.1001/jama.1993.03500240074029
Text Size: A A A
Published online
Article
References

Objective.  —To test the a priori hypotheses that significant bone loss occurs in lactation of greater than 5 months' duration and that bone mass returns to baseline levels when breast-feeding ceases.

Design.  —Prospective cohort study design of 12 months' duration.

Setting.  —General community setting with recruitment occurring at birthing education classes.

Participants.  —Volunteer sample of 98 healthy women of white (n=95) and Asian (n=3) origin, aged 20 to 40 years, and 0 to 1 parity prior to parturition, grouped according to lactation duration: 0 through 1, 2 through 5, and 6 or more months.

Main Outcome Measures.  —Bone mineral density (BMD) of the proximal femur was measured by dual-energy x-ray densitometry at 2 weeks (baseline), 2 months, 4 months, 6 months, and 12 months following parturition, and BMD of the lumbar spine was measured at baseline, 6 months, and 12 months after parturition.

Results.  —Women with lactation duration of 6 months or longer had mean BMD losses of 5.1% and 4.8% at the lumbar spine and femoral neck, respectively, comparing baseline values with those at 6 months post partum. Women who breast-fed 0 through 1 month lost no BMD at either bone site. Bone loss in women who breast-fed 6 months or longer was not explained by differences in age, diet, body size, or physical activity. Among women who breast-fed 6 months or longer, there was evidence of return to baseline levels of the lumbar spine at 12 months after parturition. The BMD of the lumbar spine of those women who continued to breast-feed more than 9 months had increased but was still significantly lower than baseline.

Conclusion.  —Extended lactation (≥70% of energy intake is provided for ≥6 months) is associated with bone loss; however, there is evidence of return to baseline BMD measurement at 12 months after parturition.(JAMA. 1993;269:3130-3135)

REFERENCES

1 +
Johnston CC, Hui SL, Wiske P, Norton JA Jr, Epstein S.  Bone mass at maturity and subsequent rates of loss as determinants of osteoporosis.  In: DeLuca HF, Frost HM, Jee WSS, Johnston CC, Parfitt AM, eds. Osteoporosis: Recent Advances in Pathogenesis and Treatment . Baltimore, Md: University Park Press; 1981;:285-291.
2 +
Cummings SR, Kelsey JL, Nevitt MC, O'Dowd KJ.  Epidemiology of osteoporosis and osteoporotic fractures. Epidemiol Rev . 1985;;7:178-208.
3 +
Kumar R, Cohen WR, Epstein FH.  Vitamin D and calcium hormones in pregnancy. N Engl J Med . 1980;;302:1143-1145.
4 +
Hayslip CC, Klein TA, Wray HL, Duncan WE.  The effects of lactation on bone mineral content in healthy postpartum women. Obstet Gynecol . 1989;; 73:588-592.
5 +
Kent GN, Price RI, Gutteridge DH, et al.  Human lactation: forearm trabecular bone loss, increased bone turnover, and renal conservation of calcium and inorganic phosphate with recovery of bone mass following weaning. J Bone Min Res . 1990;;5:361-369.
6 +
Atkinson PJ, West RR.  Loss of skeletal calcium in lactating women. J Obstet Gynaecol Br . 1970;;77: 555-560.
7 +
Lamke B, Brundin J, Moberg P.  Changes of bone mineral content during pregnancy and lactation. Acta Obstet Gynecol Scand . 1977;;56:217-219.
8 +
Wardlaw GM, Pike AM.  The effect of lactation on peak adult shaft and ultradistal forearm bone mass in women. Am J Clin Nutr . 1986;;44:283-286.
9 +
Chan GM, Slater P, Ronald N, et al.  Bone mineral status of lactating mothers of different ages. Am J Obstet Gynecol . 1982;;144:438-441.
10 +
Cunningham AS, Mazess RB.  Bone-mineral loss in lactating adolescents. J Pediatr . 1983;;103:338-339.
11 +
Greer FR, Garn SM.  Loss of the bone mineral content in lactating adolescents. J Pediatr . 1982;; 101:718-719.
12 +
Goldsmith NF, Johnston JO.  Bone mineral: effects of oral contraceptives, pregnancy and lactation. J Bone Joint Surg Am . 1975;;57:657.
13 +
Frisancho AR, Garn SM, Ascoli W.  Unaltered cortical area of pregnant and lactating women. Invest Radiol . 1971;;6:119-121.
14 +
Sowers MF, Wallace RB, Lemke JH.  Correlates of forearm bone mass among women during maximal bone mineralization. Prev Med . 1985;;14: 585-596.
15 +
Alderman BW, Weiss NS, Daling JR, Ure CL, Ballard JH.  Reproductive history and postmenopausal risk of hip and forearm fracture. Am J Epidemiol . 1986;;124:262-267.
16 +
Aloia JF, Vaswani AN, Yeh JK, Ross P, Ellis K, Cohn SH.  Determinants of bone mass in postmenopausal women. Arch Intern Med . 1983;;143: 1700-1704.
17 +
Mazess RB, Collick B, Trempe J, Barden H, Hanson J.  Performance evaluation of a dual-energy x-ray bone densitometer. Calcif Tissue Int . 1989;; 44:228-232.
18 +
Price PA, Parthemore JG, Deftos LI.  New biochemical marker for bone metabolism. J Clin Invest . 1980;;66:878-883.
19 +
Batsakis JG.  Serum alkaline phosphatase: refining an old test for the future. Diagn Med . (May) 1982;:25-33.
20 +
Block G, Hartman AM, Dresser CM, Carroll MD, Gannon J, Gardner L.  A data-based approach to diet questionnaire design and testing. Am J Epidemiol . 1986;;124:453-469.
21 +
Gray GE, Gray LK.  Anthropometric measurements and their interpretation: principles, practice, problems. J Am Diet Assoc . 1980;;77:534-538.
22 +
Kushner RF, Scholler DA.  Estimation of total body water by bioelectrical impedance analysis. Am J Clin Nutr . 1986;;44:417-424.
23 +
Sallis JF, Haskell WL, Wood PD, et al.  Physical activity assessment methodology in the Five-City Project. Am J Epidemiol . 1985;;121:91-106.
24 +
Rosner B. Fundamentals of Biostatistics . Boston, Mass: Duxbury Press; 1982;.
25 +
Kleinbaum DG, Kupper LL. Applied Regression Analysis and Other Multivariable Methods . North Scituate, Mass: Duxbury Press; 1978;.
26 +
Grizzle JE, Allen DM.  Analysis of growth and dose response curves. Biometrics . 1969;;25:357-381.
27 +
Butte NF, Garza C, Stuff JE, Smith EO, Nichols BL.  Effect of maternal diet and body composition on lactational performance. Am J Clin Nutr . 1984;; 39:296-306.
28 +
Kent GN, Price RI, Gutteridge DH, et al.  The efficiency of intestinal calcium absorption is increased in late pregnancy but not in established lactation. Calcif Tissue Int . 1991;;48:293-295.
29 +
Miller MA, Omura TH, Miller SC.  Increased cancellous bone remodeling during lactation in beagles. Bone . 1989;;10:279-285.
30 +
Rowland GN, Capen CC, Young DM, et al.  Microradiographic evaluation of bone from cows with experimental hypervitaminosis D, diet-induced hypocalcemia and naturally occuring parturient paresis. Calcif Tissue Res . 1972;;9:179-193.
31 +
Benzie D, Boyne AW, Dalgarno AC, Duckworth J, Hill R, Walker DM.  Studies of skeleton of the sheep, II: the relationship between calcium intake and resorption and repair of the skeleton in pregnancy and lactation. J Agric Sci . 1956;;48:175-86.
32 +
Spencer GR.  Pregnancy and lactational osteoporosis. Am J Pathol . 1979;;95:277-280.
33 +
Ellinger BM, Duckworth J, Dalgarno AC, Quenoville MH.  Skeletal changes during pregnancy and lactation in the rat: effect of different levels of dietary calcium. Br J Nutr . 1952;;5:235-253.
34 +
Miller SC, Halloran BP, DeLuca HF, et al.  Role of vitamin D in maternal skeletal changes during pregnancy and lactation: a histomorphometric study. Calcif Tissue Int . 1982;;34:245-252.
35 +
Miller SC, Shupe JG, Redd EH, Miller MA, Omura TH.  Changes in bone mineral and bone formation rates during pregnancy and lactation in rats. Bone . 1986;;7:283-287.
36 +
Ryan AS, Rush D, Krieger FW, Lewandowski GE.  Recent declines in breast-feeding in the United States, 1984 through 1989. Pediatrics . 1991;;88: 719-727.
37 +
Termine JD.  Bone matrix proteins and the mineralization process.  In: Primer on Metabolic Bone Diseases and Disorders of Mineral Metabolism . Kelseyville, Calif: American Society for Bone and Mineral Research; 1990;:16-18.
38 +
Krukowski M.  Calcium deficiency during lactation and in the first two weeks after weaning: decreased ash and increased magnesium in bone of rat pups. Bone . 1987;;8:251-257.
39 +
Hagaman JR, Ambrose WW, Hirsch PF.  A scanning electron microscopic and photon absorptiometric study of the development, prolongation, and pattern of recovery from lactation-induced osteopenia in rats. Bone Min Res . 1990;;5:123-132.
40 +
Brommage R, DeLuca HF.  Regulation of bone mineral loss during lactation. Am J Physiol . 1985;; 248:E182-E187.
41 +
Shaaban MM, Gamal HS, Ghaneimah SA.  The recovery of ovarian function during breast-feeding. J Steroid Biochem . 1987;;21:1043-1053.
42 +
Dada OA, Laditan AAO.  Circulating hormonal levels during prolonged lactational amenorrhea. Clin Chim Acta . 1982;;123:293-302.
43 +
Baird DT, McNeilly AS, Sawers RS, Sharpe RM.  Failure of estrogen-induced discharge of luteinizing hormone in lactating women. J Clin Endocrinol Metab . 1979;;49:500-506.
44 +
Zarate A, Canales ES.  Endocrine aspects of lactation and postpartum infertility. J Steroid Biochem . 1987;;27:1023-1028.
45 +
Schlechte JA, Sherman B, Martin R.  Bone density in amenorrheic women with and without hyperprolactinemia. J Clin Endocrinol Metab . 1983;; 56:1120-1123.
46 +
Klibanski A, Neer RM, Beitins IZ, Ridgway EC, Zervas NT, McArthur JW.  Decreased bone density in hyperprolactinemic women. N Engl J Med . 1980;;303:1511-1514.
47 +
Hillman L, Sateesha S, Haussler M, Wiest W, Slatopolsky E, Haddad J.  Control of mineral homeostasis during lactation. Am J Obstet Gynecol . 1981;;139:471-476.
48 +
Greer FR, Tsang RC, Searcy JE, Levin RS, Steichen JJ.  Mineral homeostasis during lactation— relationship to serum 1,25-dihydroxyvitamin D,25-hydroxyvitamin D, parathyroid hormone and calcitonin. Am J Clin Nutr . 1982;;36:431-437.
49 +
Chan GM, McMurry M, Westover K, Engelbert-Fenton K, Thomas MR.  Effects of increased dietary calcium intake upon the calcium and bone mineral status of lactating adolescent and adult women. Am J Clin Nutr . 1987;;46:319-323.
50 +
Greer FR, Lane J, Ho M.  Elevated serum parathyroid hormone, calcitonin, and 1,25-dihydroxy-vitamin D in lactating women nursing twins. Am J Clin Nutr . 1984;;40:562-568.
51 +
Khosla S, Johansen KL, Ory SJ, O'Brien PC, Kao PC.  Parathyroid hormone-related peptide in lactation and in umbilical cord blood. Mayo Clin Proc . 1990;;65:1408-1414.
52 +
Sowers MF, Crutchfield M, Jannausch MS, Updike S, Corton G.  A prospective evaluation of bone mineral change in pregnancy. Obstet Gynecol . 1991;; 77:841-845.
53 +
Drinkwater BL, Chesnut CH.  Bone density changes during pregnancy and lactation in active women: a longitudinal study. Bone Miner . 1991;;14: 153-160.
54 +
Gertner JM, Coustan DR, Kliger AS, Mallette LE, Ravin N, Broadus AE.  Pregnancy as a state of physiologic absorptive hypercalciuria. Am J Med . 1986;;81:451-456.
55 +
Davis OK, Hawkins DS, Rubin LP, Posillico JT, Brown EM, Schiff I.  Serum parathyroid hormone (PTH) in pregnant women determined by an immunoradiometric assay for intact PTH. J Clin Endocrinol Metab . 1988;;67:850-852.

Figures

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Country-Specific Mortality and Growth Failure in Infancy and Yound Children and Association With Material Stature

Use interactive graphics and maps to view and sort country-specific infant and early dhildhood mortality and growth failure data and their association with maternal

1 +
Johnston CC, Hui SL, Wiske P, Norton JA Jr, Epstein S.  Bone mass at maturity and subsequent rates of loss as determinants of osteoporosis.  In: DeLuca HF, Frost HM, Jee WSS, Johnston CC, Parfitt AM, eds. Osteoporosis: Recent Advances in Pathogenesis and Treatment . Baltimore, Md: University Park Press; 1981;:285-291.
2 +
Cummings SR, Kelsey JL, Nevitt MC, O'Dowd KJ.  Epidemiology of osteoporosis and osteoporotic fractures. Epidemiol Rev . 1985;;7:178-208.
3 +
Kumar R, Cohen WR, Epstein FH.  Vitamin D and calcium hormones in pregnancy. N Engl J Med . 1980;;302:1143-1145.
4 +
Hayslip CC, Klein TA, Wray HL, Duncan WE.  The effects of lactation on bone mineral content in healthy postpartum women. Obstet Gynecol . 1989;; 73:588-592.
5 +
Kent GN, Price RI, Gutteridge DH, et al.  Human lactation: forearm trabecular bone loss, increased bone turnover, and renal conservation of calcium and inorganic phosphate with recovery of bone mass following weaning. J Bone Min Res . 1990;;5:361-369.
6 +
Atkinson PJ, West RR.  Loss of skeletal calcium in lactating women. J Obstet Gynaecol Br . 1970;;77: 555-560.
7 +
Lamke B, Brundin J, Moberg P.  Changes of bone mineral content during pregnancy and lactation. Acta Obstet Gynecol Scand . 1977;;56:217-219.
8 +
Wardlaw GM, Pike AM.  The effect of lactation on peak adult shaft and ultradistal forearm bone mass in women. Am J Clin Nutr . 1986;;44:283-286.
9 +
Chan GM, Slater P, Ronald N, et al.  Bone mineral status of lactating mothers of different ages. Am J Obstet Gynecol . 1982;;144:438-441.
10 +
Cunningham AS, Mazess RB.  Bone-mineral loss in lactating adolescents. J Pediatr . 1983;;103:338-339.
11 +
Greer FR, Garn SM.  Loss of the bone mineral content in lactating adolescents. J Pediatr . 1982;; 101:718-719.
12 +
Goldsmith NF, Johnston JO.  Bone mineral: effects of oral contraceptives, pregnancy and lactation. J Bone Joint Surg Am . 1975;;57:657.
13 +
Frisancho AR, Garn SM, Ascoli W.  Unaltered cortical area of pregnant and lactating women. Invest Radiol . 1971;;6:119-121.
14 +
Sowers MF, Wallace RB, Lemke JH.  Correlates of forearm bone mass among women during maximal bone mineralization. Prev Med . 1985;;14: 585-596.
15 +
Alderman BW, Weiss NS, Daling JR, Ure CL, Ballard JH.  Reproductive history and postmenopausal risk of hip and forearm fracture. Am J Epidemiol . 1986;;124:262-267.
16 +
Aloia JF, Vaswani AN, Yeh JK, Ross P, Ellis K, Cohn SH.  Determinants of bone mass in postmenopausal women. Arch Intern Med . 1983;;143: 1700-1704.
17 +
Mazess RB, Collick B, Trempe J, Barden H, Hanson J.  Performance evaluation of a dual-energy x-ray bone densitometer. Calcif Tissue Int . 1989;; 44:228-232.
18 +
Price PA, Parthemore JG, Deftos LI.  New biochemical marker for bone metabolism. J Clin Invest . 1980;;66:878-883.
19 +
Batsakis JG.  Serum alkaline phosphatase: refining an old test for the future. Diagn Med . (May) 1982;:25-33.
20 +
Block G, Hartman AM, Dresser CM, Carroll MD, Gannon J, Gardner L.  A data-based approach to diet questionnaire design and testing. Am J Epidemiol . 1986;;124:453-469.
21 +
Gray GE, Gray LK.  Anthropometric measurements and their interpretation: principles, practice, problems. J Am Diet Assoc . 1980;;77:534-538.
22 +
Kushner RF, Scholler DA.  Estimation of total body water by bioelectrical impedance analysis. Am J Clin Nutr . 1986;;44:417-424.
23 +
Sallis JF, Haskell WL, Wood PD, et al.  Physical activity assessment methodology in the Five-City Project. Am J Epidemiol . 1985;;121:91-106.
24 +
Rosner B. Fundamentals of Biostatistics . Boston, Mass: Duxbury Press; 1982;.
25 +
Kleinbaum DG, Kupper LL. Applied Regression Analysis and Other Multivariable Methods . North Scituate, Mass: Duxbury Press; 1978;.
26 +
Grizzle JE, Allen DM.  Analysis of growth and dose response curves. Biometrics . 1969;;25:357-381.
27 +
Butte NF, Garza C, Stuff JE, Smith EO, Nichols BL.  Effect of maternal diet and body composition on lactational performance. Am J Clin Nutr . 1984;; 39:296-306.
28 +
Kent GN, Price RI, Gutteridge DH, et al.  The efficiency of intestinal calcium absorption is increased in late pregnancy but not in established lactation. Calcif Tissue Int . 1991;;48:293-295.
29 +
Miller MA, Omura TH, Miller SC.  Increased cancellous bone remodeling during lactation in beagles. Bone . 1989;;10:279-285.
30 +
Rowland GN, Capen CC, Young DM, et al.  Microradiographic evaluation of bone from cows with experimental hypervitaminosis D, diet-induced hypocalcemia and naturally occuring parturient paresis. Calcif Tissue Res . 1972;;9:179-193.
31 +
Benzie D, Boyne AW, Dalgarno AC, Duckworth J, Hill R, Walker DM.  Studies of skeleton of the sheep, II: the relationship between calcium intake and resorption and repair of the skeleton in pregnancy and lactation. J Agric Sci . 1956;;48:175-86.
32 +
Spencer GR.  Pregnancy and lactational osteoporosis. Am J Pathol . 1979;;95:277-280.
33 +
Ellinger BM, Duckworth J, Dalgarno AC, Quenoville MH.  Skeletal changes during pregnancy and lactation in the rat: effect of different levels of dietary calcium. Br J Nutr . 1952;;5:235-253.
34 +
Miller SC, Halloran BP, DeLuca HF, et al.  Role of vitamin D in maternal skeletal changes during pregnancy and lactation: a histomorphometric study. Calcif Tissue Int . 1982;;34:245-252.
35 +
Miller SC, Shupe JG, Redd EH, Miller MA, Omura TH.  Changes in bone mineral and bone formation rates during pregnancy and lactation in rats. Bone . 1986;;7:283-287.
36 +
Ryan AS, Rush D, Krieger FW, Lewandowski GE.  Recent declines in breast-feeding in the United States, 1984 through 1989. Pediatrics . 1991;;88: 719-727.
37 +
Termine JD.  Bone matrix proteins and the mineralization process.  In: Primer on Metabolic Bone Diseases and Disorders of Mineral Metabolism . Kelseyville, Calif: American Society for Bone and Mineral Research; 1990;:16-18.
38 +
Krukowski M.  Calcium deficiency during lactation and in the first two weeks after weaning: decreased ash and increased magnesium in bone of rat pups. Bone . 1987;;8:251-257.
39 +
Hagaman JR, Ambrose WW, Hirsch PF.  A scanning electron microscopic and photon absorptiometric study of the development, prolongation, and pattern of recovery from lactation-induced osteopenia in rats. Bone Min Res . 1990;;5:123-132.
40 +
Brommage R, DeLuca HF.  Regulation of bone mineral loss during lactation. Am J Physiol . 1985;; 248:E182-E187.
41 +
Shaaban MM, Gamal HS, Ghaneimah SA.  The recovery of ovarian function during breast-feeding. J Steroid Biochem . 1987;;21:1043-1053.
42 +
Dada OA, Laditan AAO.  Circulating hormonal levels during prolonged lactational amenorrhea. Clin Chim Acta . 1982;;123:293-302.
43 +
Baird DT, McNeilly AS, Sawers RS, Sharpe RM.  Failure of estrogen-induced discharge of luteinizing hormone in lactating women. J Clin Endocrinol Metab . 1979;;49:500-506.
44 +
Zarate A, Canales ES.  Endocrine aspects of lactation and postpartum infertility. J Steroid Biochem . 1987;;27:1023-1028.
45 +
Schlechte JA, Sherman B, Martin R.  Bone density in amenorrheic women with and without hyperprolactinemia. J Clin Endocrinol Metab . 1983;; 56:1120-1123.
46 +
Klibanski A, Neer RM, Beitins IZ, Ridgway EC, Zervas NT, McArthur JW.  Decreased bone density in hyperprolactinemic women. N Engl J Med . 1980;;303:1511-1514.
47 +
Hillman L, Sateesha S, Haussler M, Wiest W, Slatopolsky E, Haddad J.  Control of mineral homeostasis during lactation. Am J Obstet Gynecol . 1981;;139:471-476.
48 +
Greer FR, Tsang RC, Searcy JE, Levin RS, Steichen JJ.  Mineral homeostasis during lactation— relationship to serum 1,25-dihydroxyvitamin D,25-hydroxyvitamin D, parathyroid hormone and calcitonin. Am J Clin Nutr . 1982;;36:431-437.
49 +
Chan GM, McMurry M, Westover K, Engelbert-Fenton K, Thomas MR.  Effects of increased dietary calcium intake upon the calcium and bone mineral status of lactating adolescent and adult women. Am J Clin Nutr . 1987;;46:319-323.
50 +
Greer FR, Lane J, Ho M.  Elevated serum parathyroid hormone, calcitonin, and 1,25-dihydroxy-vitamin D in lactating women nursing twins. Am J Clin Nutr . 1984;;40:562-568.
51 +
Khosla S, Johansen KL, Ory SJ, O'Brien PC, Kao PC.  Parathyroid hormone-related peptide in lactation and in umbilical cord blood. Mayo Clin Proc . 1990;;65:1408-1414.
52 +
Sowers MF, Crutchfield M, Jannausch MS, Updike S, Corton G.  A prospective evaluation of bone mineral change in pregnancy. Obstet Gynecol . 1991;; 77:841-845.
53 +
Drinkwater BL, Chesnut CH.  Bone density changes during pregnancy and lactation in active women: a longitudinal study. Bone Miner . 1991;;14: 153-160.
54 +
Gertner JM, Coustan DR, Kliger AS, Mallette LE, Ravin N, Broadus AE.  Pregnancy as a state of physiologic absorptive hypercalciuria. Am J Med . 1986;;81:451-456.
55 +
Davis OK, Hawkins DS, Rubin LP, Posillico JT, Brown EM, Schiff I.  Serum parathyroid hormone (PTH) in pregnant women determined by an immunoradiometric assay for intact PTH. J Clin Endocrinol Metab . 1988;;67:850-852.

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