Harriet H. Cloud

Myriam Peralta‐Carcelen

Myriam Peralta-Carcelen

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Should human milk for premature children be fortified after discharge to improve neurodevelopmental outcomes?

Jornal de Pediatria (Versão em Português)

Peralta-Carcelen, Myriam

Cloud, Harriet H.

Elsevier - Publisher Connector 

Should human milk for premature children be fortified after discharge to improve neurodevelopmental outcomes? 

Peralta‐Carcelen, Myriam

J Pediatr (Rio J). 2016;92(2):111--112
www.jped.com.br
EDITORIAL
Should  human  milk  for  premature  children  be fortiﬁed
after discharge  to  improve  neurodevelopmental
outcomes?,
O  leite  materno  deve  ser  fortiﬁcado  para  crianc¸as prematuras  após  terem
alta  para  melhorar  os  resultados  de  neurodesenvolvimento?
Myriam Peralta-Carcelena,∗, Harriet H. Cloudb
a University  of  Alabama  at  Birmingham  (UAB),  Birmingham,  United  States
b
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sDepartment  of  Nutrition  and  Sciences,  University  of  Alabama
Preterm  children  are  at  higher  risk  for  neurodevelopmental
problems.1 Exclusive  breastfeeding  for  all  children,  includ-
ing  term  infants,  has  been  recommended  for  the  health
beneﬁts  as  well  as  overall  wellbeing.2 In  addition,  improved
developmental  outcomes  have  been  reported  in  term  chil-
dren  who  are  exclusively  breastfed.3 In  preterm  children,
the  advantages  of  human  milk  have  been  well  estab-
lished  for  protection  against  necrotizing  enterocolitis  and
sepsis,  and  trophic  effects.4 However,  it  has  been  recog-
nized  that,  in  preterm  children,  human  milk  alone  may
not  support  optimal  growth  because  of  insufﬁcient  nutrient
content.5 Preterm  infants  are  born  at  a  period  of  signiﬁ-
cant  organ  development  and  are  at  risk  for  deﬁciency  of
essential  nutrients  and  trophic  factors  that  promote  growth
and  brain  development,  such  as  long-chain  polyunsatu-
rated  fatty  acids  and  possibly  others.6 Without  fortiﬁcation,
preterm  children  may  have  growth  retardation,  which  has
been  associated  with  impaired  neurodevelopment.7 There-
fore,  it  has  been  recommended  that  all  preterm  infants
 Please cite this article as: Peralta-Carcelen M, Cloud HH.
Should human milk for premature children be fortiﬁed after dis-
charge to improve neurodevelopmental outcomes? J Pediatr (Rio
J). 2016;92:111--2.
 See paper by da Cunha et al. in pages 136--42.
∗ Corresponding author.
E-mail: mperalta@peds.uab.edu (M. Peralta-Carcelen).
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http://dx.doi.org/10.1016/j.jped.2016.01.001
0021-7557/© 2016 Sociedade Brasileira de Pediatria. Published by Elseviirmingham  (UAB),  Birmingham,  United  States
ith  birth  weight  <1800  g  should  receive  fortiﬁed  human
ilk,  to  add  supplemental  nutrient  fortiﬁcation,  focusing
n  proteins  and  minerals,  and  vitamins  in  particular  dur-
ng  the  neonatal  intensive  care  unit  stay  to  assure  adequate
rowth.8 This  fortiﬁcation  has  been  provided  with  differ-
nt  commercially  available  components,  and  the  quality
f  available  products  varies.  Some  units  use  a  more  stan-
ardized  approached  while  others  use  a  more  individualized
pproach.9
Improved  neurodevelopmental  outcome  and  the  use  of
uman  milk  in  preterm  children  has  been  reported  in  large,
ostly  observational  retrospective  studies10;  a  more  recent
eview  did  not  conclude  that  there  was  improved  neurode-
elopmental  outcome  with  the  use  of  human  milk  in  preterm
hildren  in  their  meta-analyses.11 However,  in  that  review,
tudies  included  did  not  have  much  information  on  fortiﬁer
se.  A  study12 reported  a  paradox  between  preterm  infants
ed  with  human  milk  that  grew  less  during  hospitalization
ompared  to  formula  fed  infants,  but  had  better  neurode-
elopment  in  the  ﬁrst  few  years  of  life;  however,  the  group
hat  was  breastfed  had  higher  birth  weight,  although  the
uthors  controlled  for  growth  restriction  and  socioeconomic
tatus.
Use  of  fortiﬁed  human  milk  during  the  NICU  stay  has
emonstrated  improvement  in  growth  in  preterm  infants12;
owever,  studies  on  long  term  neurodevelopmental  outcome
re  not  conclusive.  A  review  looked  speciﬁcally  for  effects  of
uman  milk  fortiﬁcation  after  discharge  on  development13
er Editora Ltda. All rights reserved.
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112  
nd  did  not  ﬁnd  differences  in  neurodevelopmental  out-
ome.
There  are  several  human  milk  fortiﬁers  that  had  been
romoted  for  use  with  human  milk  in  premature  infants5;
n  addition,  some  hospitals  use  powdered  preterm  formula
n  order  to  provide  minerals  and  other  needed  nutrients  for
reterm  children.  The  cost  of  commercially  available  for-
iﬁers  is  high,  in  addition  to  problems  with  adding  possible
ontamination  or  excessive  use  of  fortiﬁers  and  effects  on
ong-term  health.
The  present  article  from  da  Cunha  et  al.14 reports  on
 randomized  clinical  trial  of  a  formula  powder  (NESTLÉ®,
evey,  Switzerland)  human  milk  vs.  human  milk  with  no
upplementation  on  infants  born  weighing  less  than  1500  g
fter  being  discharged  from  the  nursery.  This  study  has  mul-
iple  strengths,  such  as  using  a  valid  randomized  design
nd  blinding  developmental  evaluators  to  the  interven-
ion  group.  However,  there  are  several  variables  that  will
e  difﬁcult  to  control  for.  Preterm  infants  represent  a
eterogeneous  population  who  may  require  carefully  indi-
idualized  nutritional  care.  In  addition,  there  is  large
ariation  between  the  content  of  breast  milk  from  one
other  to  another.  Although  this  was  a  randomized  study,
uman  milk  content  was  not  analyzed;  therefore,  a  great
ariability  across  the  different  mothers  included  in  the  study
s  possible.  If  higher-quality  fortiﬁers  and  maternal  vitamin
nd  mineral  supplementation  were  used,  the  results  may
ave  been  statistically  signiﬁcant  between  groups.
Although  not  described  in  the  study,  we  can  assume  that
nfants  were  fed  directly  at  the  breast,  and  only  supple-
ented  children  received  expressed  breast  milk  by  other
eans.
This  study  addresses  an  important  question  regarding
hether  fortiﬁcation  of  human  milk  should  be  recommended
ost-discharge  for  preterm  infants  for  the  theoretical  advan-
ages  of  higher  protein  and  nutrient  content  to  improve
eurodevelopmental  outcomes.  This  becomes  particularly
mportant  for  infants  born  at  extreme  prematurity  with
onger  hospitalization,  who  may  have  a  signiﬁcant  accumu-
ated  deﬁcit  in  nutrients  prior  to  discharge.  It  is  possible  that
ith  newer  guidelines  of  fortiﬁcation  during  the  NICU  stay,
hildren  may  not  be  as  a  disadvantage  as  we  had  assumed
reviously.  Several  investigations  are  ongoing,  looking  into
he  quality  and  duration  of  human  milk  fortiﬁcation.  In
ddition,  fortiﬁcation  after  discharge  is  not  without  difﬁcul-
ies,  considering  the  high  cost  of  multicomponent  fortiﬁers;
erhaps  limited  availability;  possible  contamination  during
ixing,  in  particular  in  areas  with  limited  resources;  and,
erhaps,  even  the  discouragement  of  breastfeeding  when
nfants  are  at  home.
We  are  left  with  the  question  of  whether  we  need  to
ortify  breast  milk  for  preterm  infants  after  discharge  to
mprove  neurodevelopmental  outcomes;  however,  we  can  be
1Peralta-Carcelen  M,  Cloud  HH.
eassured  from  this  study  that  if  there  is  a  clinical  indication
or  fortiﬁcation,  it  must  not  interfere  with  exclusive  breast-
eeding  --  the  desired  method  of  feeding  preterm  infants  --
iven  all  the  advantages  that  breastfeeding  provides.
onﬂicts of  interest
he  authors  declare  no  conﬂicts  of  interest.
eferences
1. Stephens BE, Vohr BR. Neurodevelopmental outcome of the pre-
mature infant. Pediatr Clin North Am. 2009;56:631--46.
2. Fewtrell MS, Morgan JB, Duggan C, Gunnlaugsson G, Hibberd
PL, Lucas A, et al. Optimal duration of exclusive breastfeeding:
what is the evidence to support current recommendations? Am
J Clin Nutr. 2007;85:635S--8S.
3. Gertosio C, Meazza C, Pagani S, Bozzola M. Breast feeding:
gamut of beneﬁts. Minerva Pediatr. 2015, May [Epub ahead of
print].
4. Johnson TJ, Patel AL, Bigger HR, Engstrom JL, Meier PP. Cost
savings of human milk as a strategy to reduce the incidence
of necrotizing enterocolitis in very low birth weight infants.
Neonatology. 2015;107:271--6.
5. Ziegler EE. Human milk and human milk fortiﬁers. World Rev
Nutr Diet. 2014;110:215--27.
6. Anderson A, Swank P, Wildin S, Landry S, Smith K. Modeling
analysis of change in neurologic abnormalities in children born
prematurely: a novel approach. J Child Neurol. 1999;14:502--8.
7. Ehrenkranz RA. Nutrition, growth and clinical outcomes. World
Rev Nutr Diet. 2014;110:11--26.
8. Moro GE, Arslanoglu S, Bertino E, Corvaglia L, Montirosso
R, Picaud JC, et al. XII. Human milk in feeding premature
infants: consensus statement. J Pediatr Gastroenterol Nutr.
2015;61:S16--9.
9. Arslanoglu S. IV. Individualized fortiﬁcation of human milk:
adjustable fortiﬁcation. J Pediatr Gastroenterol Nutr.
2015;61:S4--5.
0. Vohr BR, Poindexter BB, Dusick AM, McKinley LT, Higgins RD,
Langer JC, et al. Persistent beneﬁcial effects of breast milk
ingested in the neonatal intensive care unit on outcomes of
extremely low birth weight infants at 30 months of age. Pedi-
atrics. 2007;120:e953--9.
1. Koo W, Tank S, Martin S, Shi R. Human milk and neurodevel-
opment in children with very low birth weight: a systematic
review. Nutr J. 2014;13:94.
2. Kuschel CA, Harding JE. Multicomponent fortiﬁed human
milk for promoting growth in preterm infants. CDS Rev.
2004;1:CD000343.
3. Young L, Embleton ND, McCormick FM, McGuire W. Multinutrient
fortiﬁcation of human breast milk for preterm infants following
hospital discharge. CDS Rev. 2013;2:CD004866.4. da Cunha RD, Lamy Filho F, Rafael EV, Lamy ZC, de Queiroz AL.
Breast milk supplementation and preterm infant development
after hospital discharge: a randomized clinical trial. J Pediatr
(Rio J). 2016;92:136--42.


J Pediatr (Rio J). 2016;92(2):111--112
www.jped.com.br
EDITORIAL
Should  human  milk  for  premature  children  be fortiﬁed
after discharge  to  improve  neurodevelopmental
outcomes?,
O  leite  materno  deve  ser  fortiﬁcado  para  crianc¸as prematuras  após  terem
alta  para  melhorar  os  resultados  de  neurodesenvolvimento?
Myriam Peralta-Carcelena,∗ e Harriet H. Cloudb
a University  of  Alabama  at  Birmingham  (UAB),  Birmingham,  Estados  Unidos
b Departamento  de  Nutric¸ão  e  Ciências,  University  of  Alabama  at  Birmingham  (UAB),  Birmingham,  Estados  Unidos
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dCrianc¸as prematuras  apresentam  maior  risco  de  problemas
de  neurodesenvolvimento.1 O  aleitamento  materno  exclu-
sivo  para  todas  as  crianc¸as,  inclusive  nascidos  a  termo,
foi  recomendado  para  a  obtenc¸ão  de  benefícios  à  saúde,
bem  como  para  o  bem-estar  geral.2 Além  disso,  a  melho-
ria  dos  resultados  do  desenvolvimento  foi  relatada  em
crianc¸as  nascidas  a  termo  exclusivamente  amamentadas.3
Em  crianc¸as prematuras,  as  vantagens  do  leite  materno
para  a  protec¸ão contra  enterocolite  necrosante  e  sepse
e  seus  efeitos  tróﬁcos  foram  bem  estabelecidos.4 Entre-
tanto,  foi  reconhecido  que  em  crianc¸as prematuras  somente
o  leite  materno  pode  não  favorecer  o  crescimento  ideal,
devido  ao  índice  insuﬁciente  de  nutrientes  nessas  crianc¸as.5
Neonatos  prematuros  nascem  em  um  período  de  desen-
volvimento  signiﬁcativo  dos  órgãos  e  estão  em  risco  de
DOI se refere ao artigo:
http://dx.doi.org/10.1016/j.jped.2016.01.001
 Como citar este artigo: Peralta-Carcelen M, Cloud HH. Should
human milk for premature children be fortiﬁed after discharge
to improve neurodevelopmental outcomes? J Pediatr (Rio J).
2016;92:111--2.
 Ver artigo de da Cunha et al. nas páginas 136--42.
∗ Autor para correspondência.
E-mail: mperalta@peds.uab.edu (M. Peralta-Carcelen).
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2255-5536/© 2016 Sociedade Brasileira de Pediatria. Publicado por Elseveﬁciência  de  nutrientes  essenciais  e  fatores  tróﬁcos  que
romovem  o  crescimento  e  o  desenvolvimento  do  cérebro,
omo  o  uso  de  ácidos  graxos  poli-insaturados  de  cadeia  longa
 possivelmente  outros.6 Sem  o fortiﬁcante,  as  crianc¸as
rematuras  poderão  ter  retardo  do  crescimento,  que  tem
ido  associado  com  o  neurodesenvolvimento  prejudicado.7
ortanto,  tem  sido  recomendado  que  todos  os  neonatos  pre-
aturos  com  peso  ao  nascer  <  1.800  g  devem  receber  leite
aterno  fortiﬁcado,  adicionar  uma  fortiﬁcac¸ão  de  nutrien-
es  complementares,  com  foco  em  proteínas  e  minerais,
 principalmente  vitaminas,  durante  a  estada  na  unidade
e  terapia  intensiva  neonatal  para  garantir  o  crescimento
dequado.8 Esse  fortiﬁcante  recebeu  diferentes  componen-
es  comercialmente  disponíveis  e  produtos  disponíveis  de
iferentes  qualidades.  Algumas  unidades  usam  uma  abor-
agem  mais  padronizada,  ao  passo  que  outras  usam  uma
bordagem  mais  individualizada.9
A  melhoria  do  resultado  do  neurodesenvolvimento  e  o
so  de  leite  materno  para  crianc¸as prematuras  foram  rela-
ados  em  grandes  estudos  retrospectivos  majoritariamente
bservacionais;10 uma  análise  mais  recente  não  concluiu
ue  houve  melhoria  do  resultado  do  neurodesenvolvimento
uanto  ao  uso  de  leite  materno  para  crianc¸as prematuras
m  suas  metanálises.11 Contudo,  nessa  análise,  os  estudos
ncluídos  não  tinham  muitas  informac¸ões  sobre  o  uso  de  for-
iﬁcantes.  Um  estudo12 relatou  um  paradoxo  entre  neonatos
ier Editora Ltda. Todos os direitos reservados.
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112  
rematuros  com  leite  materno  que  crescem  menos  durante
 internac¸ão  em  comparac¸ão  com  neonatos  alimentados
om  fórmulas,  porém  com  melhor  neurodesenvolvimento
os  primeiros  anos  de  vida;  contudo,  o  grupo  amamentado
presentou  maior  peso  ao  nascer,  apesar  do  controle  de
estric¸ão  de  crescimento  e  da  situac¸ão socioeconômica.
O  uso  de  fortiﬁcantes  no  leite  materno  durante  a  estada
a  unidade  de  terapia  intensiva  neonatal  (UTIN)  apresentou
elhoria  no  crescimento  em  neonatos  prematuros;12 con-
udo,  estudos  sobre  resultados  do  neurodesenvolvimento  de
ongo  prazo  não  são  conclusivos.  Uma  análise  observou  espe-
iﬁcamente  os  efeitos  de  fortiﬁcantes  no  leite  materno  após
 alta  com  relac¸ão ao  desenvolvimento13 e  não  encontrou
iferenc¸as  no  resultado  do  neurodesenvolvimento.
Existem  fortiﬁcantes  de  leite  materno  divulgados  para
so  em  leite  materno  de  neonatos  prematuros;5 além  disso,
lguns  hospitais  usam  fórmulas  em  pó  para  prematuros
ara  fornecer  minerais  e  outros  nutrientes  necessários  para
rianc¸as  prematuras.  O  custo  dos  fortiﬁcantes  comercial-
ente  disponíveis  é  alto,  além  dos  problemas  com  uma
ossível  contaminac¸ão ou  o  uso  excessivo  de  fortiﬁcantes
 os  efeitos  sobre  a  saúde  no  longo  prazo.
Esse  artigo  de  da  Cunha  et  al.14 relata  um  ensaio  clínico
andomizado  que  usa  uma  fórmula  em  pó  (Nestlé®,  Vevey,
uíc¸a)  no  leite  materno  em  comparac¸ão  com  o  leite  materno
em  suplementac¸ão em  neonatos  inferiores  a  1.500  g  após
erem  alta  do  berc¸ário.  Esse  estudo  tem  diversos  pontos
ortes,  como  usar  um  modelo  randomizado  válido  e  avali-
dores  de  desenvolvimento  cegos  em  relac¸ão ao  grupo  de
ntervenc¸ão.  Entretanto,  existem  variáveis  que  serão  difí-
eis  de  controlar.  Neonatos  prematuros  representam  uma
opulac¸ão  heterogênea  cujo  cuidado  nutricional  poderá  ter
e  ser  cuidadosamente  individualizado.  Além  disso,  há  uma
rande  variac¸ão entre  o  conteúdo  do  leite  materno  de  uma
ãe  para  outra.  Embora  tenha  sido  um  estudo  randomizado,
 conteúdo  do  leite  materno  não  foi  analisado,  portanto  é
ossível  uma  grande  variabilidade  entre  as  diferentes  mães
ncluídas  no  estudo.  Se  foram  usados  fortiﬁcantes  de  maior
ualidade  e  suplementac¸ão de  vitaminas  e  minerais  do  leite
aterno,  os  resultados  poderão  ter  sido  estatisticamente
igniﬁcativos  entre  os  grupos.
Embora  não  descrito  no  estudo,  podemos  supor  que  os
eonatos  foram  alimentados  diretamente  no  peito  e  apenas
rianc¸as  suplementadas  receberam  leite  materno  extraído
or  outros  meios.
Este  estudo  aborda  uma  importante  questão  sobre  se
 fortiﬁcac¸ão  do  leite  materno  deve  ser  recomendada
pós  a  alta  para  neonatos  prematuros  pelas  vantagens
eóricas  de  mais  proteína  e  conteúdo  de  nutrientes  para
elhorar  os  resultados  de  neurodesenvolvimento.  Isso  se
orna  particularmente  importante  em  neonatos  nascidos
m  prematuridade  extrema  com  internac¸ão  mais  longa  que
oderão  ter  um  déﬁcit  acumulado  signiﬁcativo  de  nutrien-
es  antes  da  alta.  É  possível  que,  com  diretrizes  mais  novas
obre  fortiﬁcac¸ão  durante  a  estada  na  UTIN,  as  crianc¸as
ão  estejam  em  desvantagem,  como  presumimos.  Várias
nvestigac¸ões  são  contínuas  e  visam  à  qualidade  e  durac¸ão
a  fortiﬁcac¸ão  de  leite  materno.  Além  disso,  a  fortiﬁcac¸ão
pós  a  alta  tem  suas  diﬁculdades,  considerando  o  alto  custo
os  fortiﬁcantes  com  multicomponentes,  talvez  disponibili-
ade  limitada  e  possível  contaminac¸ão durante  a  mistura,
1Peralta-Carcelen  M,  Cloud  HH
rincipalmente  em  áreas  com  recursos  limitados  e,  talvez,
té  mesmo  desencorajando  o  aleitamento  materno  quando
s  neonatos  estão  em  casa.
Resta-nos  a  dúvida  sobre  se  é  necessário  fortiﬁcar  o
eite  materno  para  neonatos  prematuros  após  a  alta  para
elhorar  os  resultados  de  neurodesenvolvimento.  Contudo,
odemos  ﬁcar  tranquilos  com  esse  estudo:  se  existe  uma
ndicac¸ão  clínica  para  fotiﬁcac¸ão,  isso  não  deve  interfe-
ir  no  aleitamento  materno  exclusivo,  método  desejado  de
limentac¸ão  de  prematuros  considerando  todas  as  vantagens
ue  a  aleitamento  materno  fornece.
onﬂitos de interesse
s  autores  declaram  não  haver  conﬂitos  de  interesse.
eferências
1. Stephens BE, Vohr BR. Neurodevelopmental outcome of the pre-
mature infant. Pediatr Clin North Am. 2009;56:631--46.
2. Fewtrell MS, Morgan JB, Duggan C, Gunnlaugsson G, Hibberd
PL, Lucas A, et al. Optimal duration of exclusive breastfeeding:
what is the evidence to support current recommendations? Am
J Clin Nutr. 2007;85:635S--8S.
3. Gertosio C, Meazza C, Pagani S, Bozzola M. Breast feeding:
gamut of beneﬁts. Minerva Pediatr. 2015, May [Epub ahead of
print].
4. Johnson TJ, Patel AL, Bigger HR, Engstrom JL, Meier PP. Cost
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Should human milk for premature children be fortified after discharge to improve neurodevelopmental outcomes?

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