Home Endocrinologia Senescenza ovarica precoce (POF, Premature Ovarian Failure)

Senescenza ovarica precoce (POF, Premature Ovarian Failure)

Premature ovarian failure

Da dottvolpicelli

 Ultimo aggiornamento 12/09/2023

Definizione: il termine menopausa deriva dal greco “μήν μηνός” (mese) e “παὒσις” (cessazione) e indica appunto la fine del ciclo mestruale e dell’età fertile della donna. Dall’epoca dei Greci e dei Romani le donne vanno in menopausa all’età di 51 anni circa.  La menopausa precoce è la cessazione delle mestruazioni, con il suo corredo sintomatologico ed endocrino-metabolico,  prima dei 40 anni di età (1).  Fuller Albright et al. nel 1942 per primi riportarono il caso di una giovane donna affetta da tale sindrome. Escluse le cause chirurgiche, la menopausa precoce è dovuta a un esaurimento ovarico precoce (POF, Premature Ovarian Failure) con cui si identifica. Alla pubertà le ovaie possiedono circa 400.000 follicoli sufficienti per 400 ovulazioni cioè per 40 anni circa di vita fertile.

Indipendentemente dall’eziologia, la POF si evidenzia con amenorrea secondaria, sintomatologia vasomotoria da deprivazione estrogenica, elevati livelli sierici di FSH ed LH e depressione dei livelli sierici di estradiolo, β-Inibina e AMH in correlazione con la diminuzione e arresto della funzionalità follicolare. Nelle fasi iniziali è presente una residua funzionalità ovarica con episodiche ovulazioni e mestruazioni anche in presenza delle citate anormalità endocrine (2,3).

Frequenza:

Interessa circa l’1-4% della popolazione mondiale (3-4).

Etiologia:
1. Idiopatica: nella quasi totalità dei casi l’eziologai non è identificabile con certezza nonostante ricerche mirate; (42).

2. Difetti genetici del cromosoma X: (S. Turner 45,X e turneriane, S. X fragile) con conseguente perdita dell’enzima 17-α-idrossilasi, enzima che converte il testosterone in estradiolo e l’androstenedione in estrone (43).

3. patologia ovarica autoimmune che causa distruzione del patrimonio follicolare ovarico (46-48) e può essere distinta in:
• Auto-anticorpi anti-ovaio (53)
• Auto-anticorpi verso i recettori ovarici delle gonadotropine
Sindrome polighiandolare autoimmune

4. Patologia ovarica iatrogena:
• chemioterapia: gli ovociti sono molto sensibili all’azione dei chemioterapici. Ogni mese di chemioterapia comporta una riduzione di 18 mesi di vita fertile.
• terapia radiante pelvica o “total body”
• terapia chirurgica: resezione cuneiforme eccessiva, cistectomia con eccessiva asportazione del parenchima ovarico, ovariectomia.
• virus della parotite epidemica: l’infiammazione delle gonadi se cronicizza provoca la perdita della funzionalità.

5. Difetti enzimatici:
Galattosemia: l’incapacità di metabolizzare il galattosio è responsabile dell’insorgenza della POF presente nell’81% delle pazienti affette da galattosemia (49, 50).

. Deficit di aromatasi (52)
 6.Talassemia major ed emocromatosi conseguente a scarso utilizzo del ferro da deficit di sintesi dell’eme o da eccessivo accumulo di ferro dopo trasfusioni. L’emocromatosi è molto più frequente negli uomini che nelle donne, ma in menopausa la differenza fra i due sessi si annulla per la cessazione delle mestruazioni, gravidanze e allattamenti. L’accumulo di ferro a livello gonadico induce disfunzionalità ovarica (come anche per tiroide, pancreas, fegato, cuore e cervello) e quindi ipogonadismo.
 7. Post-abortiva: Flamigni riporta tre casi di ovaio resistente, insorti dopo aborto spontaneo e regrediti spontaneamente e che hanno avuto gravidanze spontanee e mette in guardia dal fare prognosi negative senza prima avere effettuato una biopsia ovarica.
 8. Stress psico-fisici
 9. Varianti del gene della α-inibina (4)
 10. TBC dell’apparato genitale: l’infiammazione delle gonadi se cronicizzata è responsabile della perdita di funzionalità delle gonadi.
11) Prolungata terapia con Gn-RH
12. COH ripetute per metodica PMA
13. Anomalie strutturali delle gonadotropine (44-45)

14. FSH-r con anomalie genetiche: Il genotipo del recettore dell’FSH svolge un ruolo importante nel determinare la risposta ovarica ad una stimolazione con l’ormone FSH. Sono stati finora evidenziati 2 anomalie strutturali dei recettori del FSH: i polimorfismi Asn680Ser e Thr307Ala. si tratta di polimorfismi a singolo nucleotide localizzati a livello dell’esone 10 del gene FSHR (45).  

I suddetti polimorfismi sono tra loro in cosiddetto linkage disequilibrium, cioè a Ser680 è associata anche 307Ala, rendendo molto frequenti due combinazioni alleliche delle quattro possibili: Thr307”“Asn680 e Ala307”“Ser680.

Diversi studi hanno associato la variante Ser680 ad una ridotta risposta alla stimolazione ovarica a seguito di somministrazione di FSH, dovuta ad una parziale resistenza del recettore all’ormone (39). Quindi le pazienti che presentano la variante Ser680 richiedono un dosaggio maggiore di FSH ricombinante per produrre una crescita follicolare ottimale ed un’adeguata concentrazione sierica di Estradiolo. Infatti, il numero medio di fiale di FSH somministrate per ottenere una stimolazione efficace è risultato più alto nelle pazienti di genotipo Ser/Ser che nelle pazienti Asn/Ser o Asn/Asn. La variante Ser680, influenzerebbe anche i livelli sierici di Estradiolo, ridotti nelle pazienti Ser/Ser, per cui le pazienti con genotipo Asn/Asn, ottenendo dei valori di estradiolo più elevati, potrebbero presentare un rischio maggiore di OHSS, sebbene questa ipotesi è tuttora controversa. Alcuni autori hanno inoltre riscontrato una maggiore frequenza dell’allele Asn680 in forme gravi di OHSS, suggerendo che il polimorfismo Asn680Ser possa rappresentare un marker predittivo sulla gravità dei sintomi in casi di OHSS, in quanto i soggetti Asn680 sarebbero più suscettibili a forme gravi di OHSS.

Inoltre, nelle pazienti con ciclo mestruale normale e polimorfismo Ser/Ser, sono stati riscontrati valori basali di FSH significativamente più alti che nei genotipi Asn/Ser e Asn/Asn. Ciò viene spiegato con il fatto che la variante Ser/Ser del recettore dell’FSH è meno sensibile all’azione dell’FSH, e che i maggiori livelli basali di FSH costituiscono una naturale compensazione dell’organismo per determinare una normale crescita follicolare.

L’analisi del genotipo del recettore dell’FSH permette di modulare in maniera individuale la somministrazione di FSH e quindi di aumentare l’efficacia e la sicurezza della terapia. Infatti, le pazienti con un genotipo “low-responder” devono essere stimolate utilizzando un dosaggio di FSH 1.5 volte maggiore rispetto al gruppo con genotipo “high-responder”. Probabilmente questo dosaggio potrebbe essere eccessivo per il gruppo “high-responder”, e viceversa, il dosaggio ideale per questo gruppo potrebbe non risultare efficace per il gruppo “low-responder”.

 15. Fumo: le donne fumatrici sono a rischio di menopusa precoce. Sono alcune sostanze chimiche, i cosiddetti idrocarburi aromatici policiclici (PAHs) principalmente contenuti nel fumo di sigarette, che, dopo essersi legate a un particolare recettore (Ahr), attivano un gene (Bax) in grado di arrecare disturbi alla gametogenesi (39).
16. Inquinamento ambientale: emissioni di fossil fuel, alcuni tipi di scarichi industriali e solventi contenenti 2-bromopropane possono provocare menopausa precoce non per mancanza di follicoli ma per alterazione della loro funzionalità o per alterazione dei siti recettoriali ovarici per le gonadotropine.

17. Alcoolismo, Disordini alimentari, BMI <20 e BMI >35: il consumo di alcool danneggia il fegato e conseguentemente diminuisce la secrezione di SHBG  con aumento dei livelli sierici di androgeni liberi. 

18. Bassa statura

Sintomatologia:

Amenorrea secondaria
Metrorragie e menometrorragie
Sindrome pre-mestruale
Disturbi vasomotori
Osteoporosi e artrosi (5)
Tachiaritmie
Insonnia
Depressione
Secchezza cutanea e delle mucose
Secchezza vaginale
Diminuzione della libido e alopecia (6-8)

Astenia, perdita di tono muscolare, perdita di concentrazione e di memoria a causa della diminuzione dei livelli sierici di DHEA
Aumentato rischio di patologia cardiaca, tiroidite di Hashimoto, m. di Addison e malattie autoimmuni: tiroiditi autoimmuni, Sindrome polighiandolare di I e II tipo, ipoparatiroidismo, artrite reumatoide, diabete IDDM, anemia perniciosa, porpora trombocitopenica idiopatica, vitiligine, lupus sistemico eritematoso, M.  di Addison).
Disfunzioni vescicali
Diabete mellito tipo II
Ipoparatiroidismo
Artrite reumatoide
Anemia perniciosa
Vitiligine
Lupus sistemico eritematoso (SLE)

Diagnostica:

  • AMH (Anti Mϋllerian Hormone) glicoproteina secreta dai follicoli primari e dai piccoli follicoli pre-antrali (<2 mm). Mostra una correlazione inversa a quella dell’FSH. I suoi valori sierici nelle donne in età fertile (2-8 ng/ml) hanno valori costanti fra un ciclo e l’altro e  indipendenti dal giorno del ciclo. L’AMH presenta un decremento lineare con l’avanzare dell’età. Il suo decremento è più precoce ed affidabile come POF-marker rispetto a tutti i markers appresso descritti  (9). Valori sierici di AMH <1 ng/ml sono da riferire a ridotta riserva ovarica (29-32) e valori <0.5 ng/ml indicano una riduzione del 90% circa della riserva ovarica (33).
  • β-inibina glicoproteina prodotta dai follicoli pre-antrali, diminuisce in menopausa.. Valori normali oscillano fra 50 e 150 pg/ml. Il suo ruolo è quello di esercitare un feed-back negativo sulla produzione di FSH. Mostra, come l’AMH, una correlazione inversa a quella dell’FSH (9). Concentrazioni basali (3° giorno) sieriche <45 pg/ml corrispondono ad un   Pregnancy Rate del 28%; mentre concentrazioni  >45 pg/ml fanno prevedere un PR del 95%. Attualmente la sua significatività come test di screening per la diagnosi di POF è messa in dubbio dall’evidente variabilità dimostrata da un ciclo all’altro e quindi alla ß-inibina è preferito l’AMH (10,11).
  • FSH: in 3a giornata, v.n. 2-6 mUI/ml. Aumenta in caso di POF. La secrezione di FSH è inibita dalla ß-inibina e dall’estradiolo. Valori sierici in terza giornata >10 mUI/ml (v.n. 2-6 mUI/ml) indicano una senescenza ovarica precoce (25).  Come per la ß-inibina, una delle principali limitazioni nell’impiego routinario del dosaggio di FSH basale ai fini della valutazione della riserva ovarica è però  costituita dalla sua estrema variabilità  spesso tra un ciclo e l’altro in quanto la secrezione di tale ormone da parte dell’ipofisi può essere  influenzata da vari fattori (26-28)
  • E2:  diminuisce in caso di POF. Valori sierici <30 pg/ml indicano una scarsa riserva ovarica; valori sierici di E2 <20 pg/ml indicano un totale esaurimento dell’attività follicolare ed una produzione di estradiolo in modo residuale; valori di E2 >50 pg/ml indicano la presenza di attività follicolare.
  • SHBG (Sex Hormone Binding Globuline): diminuisce in caso di POF. E’ sintetizzata a livello epatico, nella donna fertile i valori sierici normali sono 40-120 nmol/l. La sua sintesi è inibita da diete ipercaloriche ed iperlipidiche, ipotiroidismo, alti livelli di insulina, IGF-1 e androgeni ed è invece stimolata da tiroxina, ipertiroidismo, Growth Hormone, estrogeni ed epatopatie. In pazienti in menopausa e con POF diminuiscono nettamente al di sotto di 20 nmol/l. Una diminuzione significativa dell’SHBG comporta un aumento significativo dell’attività androgenica periferica (acne, virilismo, PCOS) ed una diminuzione dell’attività ovarica.
  • DHEA:  ormone prodotto dal surrene. Presenta valori sierici di   3-8 ng/ml  e  diminuisce in caso di POF. Valori sierici <3 ng/ml indicano uno stato di insufficienza ovarica
  • Clomifene Challenge testdosaggio dei valori sierici  di FSH al 3° giorno del ciclo; somministrazione di 100 mg di clomifene dal 5° al 9° giorno del ciclo; dosaggio FSH al 10° giorno. Il clomifene stimola la produzione di FSH, la crescita multifollicolare, la secrezione di estradiolo e l’aumento della ß-inibina; nelle donne fertili l’innalzamento della ß-inibina provoca riabbassamento dei livelli sierici di FSH mentre nelle donne con ridotta riserva ovarica si ha un innalzamento della secrezione di FSH a cui però non segue una buona stimolazione ovarica, una buona secrezione di ß-inibina e quindi i livelli di FSH restano alti (34-36).  
  • Conta dei follicoli antrali: conta dei piccoli follicoli (2-10 mm) dotati di liquido follicolare effettuata con sonda endovaginale al 3-5° giorno del ciclo. La presenza di un ridotto numero di follicoli antrali (tra 3 e 10 in totale nelle due ovaie) sarebbe, secondo alcuni studi, associata ad una scarsa risposta ovarica alla stimolazione ed ad una bassa probabilità di gravidanza (37). Al riguardo uno studio di Holte e coll. (38) ha evidenziato una correlazione lineare tra il numero di follicoli antrali e le percentuali di gravidanza ottenute in pazienti  sottoposte a fecondazione in vitro con percentuali comprese tra 0 e 15% nelle pazienti con una conta dei follicoli antrali compresa tra 0 e 5, pari al 16-25% nelle pazienti con conta tra 6 e 11, pari al 26-35% nelle  pazienti con conta tra 12 e 23 e maggiore del 35% nelle pazienti con conta totale dei follicoli antrali >23.
  • Volume ovarico: l’eccessiva variabilità dei risultati in rapporto ai diversi operatori, nonché la scarsa specificità rilevata nel complesso, sembrerebbero indicare uno scarso peso di tale marker nella valutazione della riserva ovarica. Nelle pazienti POF l’ovaio appare “shriveled”, “avvizzito”, “accartocciato”.

POF e FERTILITA’: la possibilità di gravidanza spontanea in tale stato è <10%. E’ possibile una ripresa sporadica spontanea dei cicli ovulatori senza alcuna terapia. Con maggiori probabilità si può avere una  ripresa transitoria di ovulazione e cicli ovulatori dopo sospensione della terapia sostitutiva estrogenica o estro-progestinica. E’ possibile indurre ovulazione (19%) mediante l’impiego di una sequenza estrogeni/HMG. Il numero di recettori ovarici per le  gonadotropine  condiziona ovviamente la risposta ovarica.  Il numero  dei  recettori per l’FSH è incrementato dagli estrogeni  mentre  il numero dei recettori per l’LH è incrementato dall’FSH. Terapia sostitutiva estrogenica transdermica iniziando con 50 mcg fino a livelli di LH prossimo allo 0; Stimolazione con HMG 150 UI al dì aumentando dopo 5 gg se necessario, ma continuando l’estrogeno-terapia fino a ovulazione perché i livelli delle gonadotropine tendono a risalire immediatamente dopo la sospensione  dell’estrogeno-terapia. Check e al.  (Fert.  Steril. maggio 1990) hanno ottenuto 8 gravidanze/100 pazienti sempre dopo innalzamento del livello sierico di E2, anche se i livelli delle gonadotropine erano alti, 68 ovulazioni/361 (16%) cicli di terapia (40).  In caso di  insuccesso somministrare progestinico 10 mg per 10 gg in modo da provocare il flusso mestruale.  Rinunciare in caso di anovulazione dopo 6 cicli di terapia. Se la soppressione veniva effettuata con analoghi  analoghi non si avevano gravidanze. Non si sono notate differenze relativamente al fattore età. La  supplementazione va effettuata con progesterone micronizzato os/vaginale o intramuscolare. Alto è il tasso di abortività probabilmente dovuto all’azione sull’endometrio degli alti livelli di estrogeni somministrati nella la fase di soppressione  oppure per LDP nonostante  la supplementazione con Progesterone. I migliori risultati si ottengono quando c’é un rialzo spontaneo dell’E2 endogeno perché significa che l’ovaio inizia a maturare autonomamente e l’HMG contribuisce alla maturazione (13,14).

Terapia:
 

  1. Pillola contraccettiva: Nelle forme iniziali si possono somministrare estro-progestinici combinati presenti nella pillola contraccettiva. Proteggono da gravidanze indesiderate, attenuano la sintomatologia da deprivazione estrogenica e inducono flussi mestruali ritmici.
  2. HRT combinata sequenziale non continua in dosi superiori a quelle per le donne in climaterio ordinario: se non ci sono controindicazione come l’ipertensione arteriosa, il diabete mellito, trombofilia ereditaria, flebiti, varicosità degli arti inferiori , epatopatie e nelle fumatrici con età >35 anni. La via transdermica è da preferire perché bypassa il circolo epatico.  Progesterone dal 15-18° al 24° giorno del ciclo: per modulare i casi di menometrorragia.
  3. DHEA (DHEA cpr 25 mg Puritans Pride, Prastera cpr, Prasterone cpr, Fidelin cpr, Fluasterone cpr) a bassi dosaggi (25 mg x 3 volte al dì fino a 100 mg nelle donne obese per almeno 2 mesi e fino a β-HCG positivo): può indurre ovulazioni spontanee, gravidanze e combatte l’astenia, l’ipotonia muscolare, la diminuzione della libido e migliora il tono dell’umore (13-19). Il meccanismo d’azione sembra estrinsecarsi attraverso un aumento del free insulin-like growth factor I e un decremento delle HDL (20). La supplementazione con DHA riduce il tasso di aborti probabilmente mediante riduzione delle aneuploidie soprattutto nelle pazienti con età >35 anni (21). Il DHA sembra efficace per migliorare l’outcome ovulatorio e gravidico in tutte le pazienti sottoposte a tecniche PMA per infertilità (15).
  4. Cortisonici: Nelle forme autoimmuni la terapia immunosoppressiva corticosteroidea é di scarso ausilio ai fini del ripristino della fertilità (41, 51).
  5. FIV/ICSI + ET con ovodonazione: in caso di fallimento della COH
  6. Crioconservazione del tessuto ovarico: può essere utilizzato nelle giovani donne a rischio di POF.
  7. Testosterone: a piccole dosi per le stesse indicazioni della somministrazione di DHA e solo in caso che non si desiderano gravidanze.
  8. SSRI (Selective Serotonin Reuptake Inhibitors): farmaci antidepressivi utilizzati per la terapia dell’ansia, depressione ed alcuni casi di insonnia. Agiscono inibendo il reuptake della serotonina (5-idrossi-triptamina, 5-HT) nelle cellule pre-sinaptiche e quindi aumentando la quantità di serotonina disponibile per i recettori post-sinaptici. Inibiscono anche il reuptake della dopamina e della nor-epinefrina. Tra i più noti farmaci in commercio ricordiamo la fluoxetina (Prozac©), la paroxetina (Daparox©).
  9. Attività fisica aerobica: 30 minuti/die di alta attività aerobica e esercizi di allungamento muscolare  aumenta i livelli sierici di HDL colesterolo, aumenta il livello di beta endorfine e previene e riduce l’obesità.
  10. Controllo del peso (BMI 20-24), attività fisica aerobica, moderazione nel consumo di alcool e caffè, dieta bilanciata da 1.500-1700 KCal circa ricca di fibre e frutta fresca, privilegiando il consumo di pesce azzurro per la quota proteica.
  11. Gn-RH-a: in caso di chemioterapia per preservare la funzionalità ovarica (54). Si somministra i.m. l’analogo del Gn-RH 3.75 mg in forma depot (Decapeptyl® depot fl 365 mg, Enantone® 365 mg fl) ogni 28 giorni iniziando una settimana prima della chemioterapia e durante tutta la chemioterapia.   L’incidenza della menopausa precoce nel gruppo triptorelina era del 8.9% vs. 25.9% del gruppo non trattato con analoghi.
Queste  pagine fanno parte del sito www.fertilitycenter.it  in internet da marzo 2011. I testi, le tabelle, i disegni e le immagini pubblicati in queste pagine sono coperte da copyright ma a disposizione di tutti per copia e riproduzione purchè venga citata la fonte con Link al sito www.fertilitycenter.it.

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  24. Jan W. van der Steeg, Pieternel Steures, Marinus J. C. Eijkemans, J. Dik F. Habbema, Peter G. A. Hompes, Frank J. Broekmans, Peter X. J. M. Bouckaert, Patrick M. M. Bossuyt, Fulco van der Veen, and Ben W. J. Mol, on behalf of the Collaborative Effort for Clinical Evaluation in Reproductive Medicine (CECERM) Study Group: “Predictive Value and Clinical Impact of Basal Follicle- Stimulating Hormone in Subfertile, Ovulatory Women”.  (J Clin Endocrinol Metab 92: 2163–2168, 2007)
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  26. Bancsi LF, Broekmans FJ, Mol BW, Habbema JD, te Velde ER.: “Performance of basal follicle-stimulating hormone in the prediction of poor ovarian response and failure to become  pregnant after in vitro fertilization: a meta-analysis”. Fertil Steril 2003;79:1091-100.
  27. Jain T, Soules MR, Collins JA.: “Comparison of basal follicle-stimulating hormone versus the clomiphene citrate challenge test for ovarian reserve screening”. Fertil Steril 2004;82:180-5
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  29. Ebner T, Sommergruber M, Moser M, Shebl O, Schreier-Lechner E, Tews G.: “Basal level of anti-Mullerian hormone is associated with oocyte quality in stimulated cycles”. Hum Reprod 2006;21:2022-6.
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  34. Hendriks DJ, Broekmans FJ, Bancsi LF, de Jong FH, Looman CW, Te Velde ER. Repeated clomiphene citrate challenge testing in the prediction of outcome in IVF: a comparison with basal markers for ovarian reserve. Hum Reprod 2005;20:163-9.
  35. Hendriks DJ, Mol BW, Bancsi LF, te Velde ER, Broekmans FJ. The clomiphene citrate challenge test for the prediction of poor ovarian response and nonpregnancy in patients undergoing in vitro fertilization: a systematic review. Fertil Steril 2006;86:807-18
  36. Hendriks DJ, Mol BW, Bancsi LF, Te Velde ER, Broekmans FJ. Antral follicle count in the prediction of poor ovarian response and pregnancy after in vitro fertilization: a meta-analysis and comparison with basal follicle-stimulating hormone level. Fertil Steril 2005;83:291-301. 54.
  37. Jan holte, Thomas Brodin, Lars Berglund, Nermin Hadziosmanovic, Matts Olovsson, Torbjorn Bergh. Antral follicle counts are strongly associated with live-birth rates after assisted reproduction, with superior treatment outcome in women with polycystic ovaries. Fertil Steril, 2011; 96: 594-9
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  39. Aittomaki K, Herva R,Stenmann UH, Juntunen K, Ylostalo P, Hovatta O et al. Clinical features of primary ovarian failure caused by a point mutation in the follicle-stimulating hormone receptor gene. J Clin Endocrinol Metab, 1996; 81: 3722-6
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  48. Sedmak DD, Hart WR, Tubbs RR. Autoimmune oophoritis: a histopathologic study of involved ovaries with immunologic characterization of the mononuclear cell infiltrate. Int J Gynecol Pathol, 1987; 6: 73-81
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  50. Waggoner DD, Buist NRM, Donnel GN. Long-term prognosis in galactosemia: results of a survey of 350 cases. J Inherit Metab Dis., 1990; 13: 802-18.
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  52. Morishima A, Grumbach MM, Simpson ER, Fisher C, Qin K. Aromatase deficiency in male and female siblings caused by a novel mutation and the physiological role of estrogens. J Clin Endocrinol Metab, 1995; 80: 3689-98
  53. Wheatcroft MJ, Toogood AA, Li TC, Cooke ID, Weetman AP. Detection of antibodies to ovarian antigens in women with premature ovarian failure. Clin Exp Immunol., 1994; 96: 122-8
  54. L Del Mastro, L Boni, A Michelotti, et al.. “Effect of the Gonadotropin-Releasing Hormone Analogue Triptorelin on the Occurrence of Chemotherapy-Induced Early Menopause in Premenopausal Women With Breast CancerA Randomized TrialFREE”. JAMA. 2011; 306 (3) :269-276. doi: 10.1001/jama.2011.991.

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