Background

The World Health Organization (WHO)[1] defines malnutrition as "the cellular imbalance between the suppl of nutrients and energ and the bod !s demand for them to ensure growth" maintenance" and specific functions#" The term protein$energ malnutrition (%&') applies to a group of related disorders that include marasmus" (washior(or" and intermediate states of marasmus$(washior(or# The term marasmus is deri)ed from the *ree( word marasmos, which means withering or wasting# 'arasmus in)ol)es inade+uate inta(e of protein and calories and is characterized b emaciation# The term (washior(or is ta(en from the *a language of *hana and means "the sic(ness of the weaning#" Williams first used the term in 1,--" and it refers to an inade+uate protein inta(e with reasonable caloric (energ ) inta(e# &dema is characteristic of (washior(or but is absent in marasmus# .tudies suggest that marasmus represents an adapti)e response to star)ation" whereas (washior(or represents a maladapti)e response to star)ation# /hildren ma present with a mi0ed picture of marasmus and (washior(or" and children ma present with milder forms of malnutrition# 1or this reason" 2elliffe suggested the term protein$calorie (energ ) malnutrition to include both entities# 3lthough protein$energ malnutrition affects )irtuall e)er organ s stem" this article primaril focuses on its cutaneous manifestations# %atients with protein$energ malnutrition ma also ha)e deficiencies of )itamins" essential fatt acids" and trace elements" all of which ma contribute to their dermatosis#

Pathophysiology
4n general" marasmus is an insufficient energ inta(e to match the bod !s re+uirements# 3s a result" the bod draws on its own stores" resulting in emaciation# 4n (washior(or" ade+uate carboh drate consumption and decreased protein inta(e lead to decreased s nthesis of )isceral proteins# The resulting h poalbuminemia contributes to

e0tra)ascular fluid accumulation# 4mpaired s nthesis of 5$lipoprotein produces a fatt li)er# %rotein$energ malnutrition also in)ol)es an inade+uate inta(e of man essential nutrients# 6ow serum le)els of zinc ha)e been implicated as the cause of s(in ulceration in man patients# 4n a 1,7, stud of 89 children with marasmus" in)estigators found that onl those children with low serum le)els of zinc de)eloped s(in ulceration# .erum le)els of zinc correlated closel with the presence of edema" stunting of growth" and se)ere wasting# The classic "mosaic s(in" and "fla( paint" dermatosis of (washior(or bears considerable resemblance to the s(in changes of acrodermatitis enteropathica" the dermatosis of zinc deficienc # 4n 9::7" 6in et al[9] stated that "a prospecti)e assessment of food and nutrient inta(e in a population of 'alawian children at ris( for (washior(or" found "no association between the de)elopment of (washior(or and the consumption of an food or nutrient#" 'arasmus and (washior(or can both be associated with impaired glucose clearance that relates to d sfunction of pancreatic beta$cells#[-] 4n utero" plastic mechanisms appear to operate" ad;usting metabolic ph siolog and adapting postnatal undernutrition and malnutrition to define whether marasmus and (washior(or will de)elop#[8] 4n 9:19" a report from Te0as noted an 1<$month$old infant with t pe 1 glutaric acidemia who had e0tensi)e des+uamati)e pla+ues" generalized nonpitting edema" and red$tinged sparse hair" with low le)els of zinc" al(aline phosphatase" albumin" and iron# This patient has a )ariation on (washior(or" and the authors suggest that it be termed acrodermatitis d smetabolica#[=] On the same note" a bo aged 1< months with t pe 1 glutaric academia suffered from zinc deficienc and ac+uired protein energ malnutrition#[=8] 1or comple0 reasons" sic(le cell anemia can predispose suffers to protein malnutrition#[==]

Epidemiology
Frequency

United States %rotein$energ malnutrition is the most common form of nutritional deficienc among patients who are hospitalized in the >nited .tates# 3s man as half of all patients admitted to the hospital ha)e malnutrition to some degree# 4n a recent sur)e in a large children!s hospital" the pre)alence of acute and chronic protein$energ malnutrition was more than one half# This is )er much a disease that occurs in 91st centur 3merica" and a case in an <$month$old child in suburban ?etroit" 'ich" was reported in 9:1:#[@] 3dditional cases of (washior(or ha)e been noted to occur in the >nited .tates# 3n interesting report of a bab with a clinical picture imitating .te)ens$2ohnson s ndrome but who in fact had (washior(or has been noted#[7] 5abies solel fed on rice mil( can de)elop (washior(or e)en in the >nited .tates# 4n a sur)e focusing on low$income areas of the >nited .tates" 99$-=A of children aged 9$@ ears were below the 1=th percentile for weight# 3nother sur)e showed that 11A of children in low$income areas had height$for$age measurements below the =th percentile# %oor growth is seen in 1:A of children in rural populations# 4n hospitalized elderl persons" up to ==A are undernourished# >p to <=A of institutionalized elderl persons are undernourished# .tudies ha)e shown that up to =:A ha)e )itamin and mineral inta(e that is less than the recommended dietar allowance and up to -:A of elderl persons ha)e below$normal le)els of )itamins and minerals# International 4n 9:::" the WHO[<] estimated that malnourished children numbered 1<1#, million (-9A) in de)eloping countries# 4n addition" an estimated 18,#@ million children ounger than = ears are malnourished when measured in terms of weight for age# 4n south central 3sia and eastern 3frica" about half the children ha)e growth retardation due to protein$energ malnutrition# This figure is = times the pre)alence in the western world# 3 cross$sectional stud of %alestinian adolescents found that ==#@@A of bo s and @8#<1A of girls had inade+uate energ inta(e" with inade+uate protein inta(e in 1=#:7A of bo s

and 8-#:<A of girls# The recommended dail allowance for micronutrients was met b less than <:A of the stud sub;ects#[,]

Mortality/Morbidity
3ppro0imatel =:A of the 1: million deaths each ear in de)eloping countries occur because of malnutrition in children ounger than = ears# 4n (washior(or" mortalit tends to decrease as the age of onset increases#

Race
?ermatologic findings appear more significant and occur more fre+uentl among dar(er$ s(inned peoples# This finding is li(el e0plained b the greater pre)alence and the increased se)erit of protein$energ malnutrition in de)eloping countries and not to a difference in racial susceptibilit #

ge
'arasmus most commonl occurs in children ounger than = ears# This period is characterized b increased energ re+uirements and increased susceptibilit to )iral and bacterial infections# Weaning (the depri)ation of breast mil( and the commencement of nourishment with other food) occurs during this high$ris( period# Weaning is often complicated b geograph " econom " h giene" public health" culture" and dietetics# 4t can be ineffecti)e when the foods introduced pro)ide inade+uate nutrients" when the food and water are contaminated" when the access to health care is inade+uate" andBor when the patient cannot access or purchase proper nourishment# 4n some studies" the protein$energ malnutrition pre)alence among elderl persons is estimated to be as high as 8A for those li)ing in the communit " =:A for those hospitalized in acute care units or geriatric rehabilitation units" and -:$8:A for those in long$term care facilities# %rotein$energ malnutrition has also been found to be a primar factor of poor prognosis in elderl persons

!istory
6ow inta(e of calories or an inabilit to absorb calories is the (e factor in the de)elopment of (washior(or# 3 )ariet of s ndromes can be associated with (washior(or#[1:] 4n children" the findings of poor weight gain or weight lossC slowing of linear growthC and beha)ioral changes" such as irritabilit " apath " decreased social responsi)eness" an0iet " and attention deficit ma indicate protein$energ malnutrition# 4n particular" the child is apathetic when undisturbed but irritable when pic(ed up# Dwashior(or characteristicall affects children who are being weaned# .igns include diarrhea and ps chomotor changes# 3dults generall lose weight" although" in some cases" edema can mas( weight loss# %atients ma describe listlessness" eas fatigue" and a sensation of coldness# *lobal impairment of s stem function is present# %atients with protein$energ malnutrition can also present with nonhealing wounds# This ma signif a catabolic process that re+uires nutritional inter)ention# 6ewandows(i et al[11] reported (washior(or and an acrodermatitis enteropathicaEli(e eruption after a distal gastric b pass surgical procedure# Dwashior(or was reported in an infant presenting with diarrhea and dermatitis" due to infantile /rohn disease#[19] The diarrhea and dermatitis impro)ed in 9 wee(s with treatment# 3 -$ ear$old child with coe0isting celiac and Hartnup disease that resulted in (washior(or" anemia" hepatitis" h poalbuminia" angular cheilitis" glossitis" con;uncti)itis and diffuse alopecia" er thematous s(in" des+uamation" erosions" and diffuse h perpigmentation was reported b .ander et al in 9::,#[1-] With the proper nutritional supplementation" these findings resol)ed# "/upping" (placing suction cups on the bod to cure disease) on the abdomen in patients with diseases resulting in abdominal swelling (eg" (washior(or) can gi)e interesting clinical presentations#[18]

Physical
4n marasmus" the child appears emaciated with mar(ed loss of subcutaneous fat and muscle wasting# The s(in is 0erotic" wrin(led" and loose# 'on(e facies secondar to a loss of buccal fat pads is characteristic of this disorder# 'arasmus ma ha)e no clinical dermatosis# Howe)er" inconsistent cutaneous findings include fine" brittle hairC alopeciaC impaired growthC and fissuring of the nails# 4n protein$energ malnutrition" more hairs are in the telogen (resting) phase than in the anagen (acti)e) phase" a re)erse of normal# Occasionall " as in anore0ia ner)osa" mar(ed growth of lanugo hair is noted# Dwashior(or t picall presents with a failure to thri)e" edema" moon facies" a swollen abdomen (potbell )" and a fatt li)er# When present" s(in changes are characteristic and progress o)er a few da s# The s(in becomes dar(" dr " and then splits open when stretched" re)ealing pale areas between the crac(s (ie" craz pa)ement dermatosis" enamel paint s(in)# This feature is seen especiall o)er pressure areas# 4n contrast to pellagra" these changes seldom occur on sun$e0posed s(in# ?epigmentation of hair causes it to be reddish ellow to white# /url hair becomes straightened# 4f periods of poor nutrition are interspersed with good nutrition" alternating bands of pale and dar( hair" respecti)el " called the flag sign" ma occur# 3lso" hairs become dr " lusterless" sparse" and brittleC the can be pulled out easil # Temporal recession and hair loss from the bac( of the head occur" li(el secondar to pressure when the child lies down# 4n some cases" loss of hair can be e0treme# Hair can also become softer and finer and appear unrul # The e elashes can undergo the same change" ha)ing a so$called broomstic( appearance# Fail plates are thin and soft and ma be fissured or ridged# 3troph of the papillae on the tongue" angular stomatitis" 0erophthalmia" and cheilosis can occur# 4nflammator bowel diseases" such as /rohn disease and ulcerati)e colitis" ma also produce s(in manifestations secondar to malnutrition#[1=]

4n elderl persons" an indicati)e sign of malnutrition is dela ed healing and an increased presence of decubitus ulcers of stage 444 or higher# Gitamin / deficienc commonl manifests in elderl persons as perifollicular hemorrhages" petechiae" gingi)al bleeding" and splinter hemorrhages" in addition to hemarthroses and subperiosteal hemorrhages# 3nemia ma result" and wound healing ma be impaired# Fiacin deficienc clinicall manifests as pellagra (ie" dermatitis" dementia" diarrhea) in ad)anced cases# The dermatitis manifests in sun$e0posed areas" including the bac(" nec( (/asal nec(lace)" face" and dorsum of the hands (gauntlet of pellagra) initiall as painful er thema and itching# .ubse+uentl " )esicles and bullae ma de)elop and erupt" creating crusted" scal lesions# 1inall " the s(in becomes rough and co)ered b dar( scales and crusts# .tri(ing demarcation of affected areas from normal s(in is noted# %rotein$energ malnutrition is also associated with an increased li(elihood of calciph la0is" a small )essel )asculopath in)ol)ing mural calcification with intimal proliferation" fibrosis" and thrombosis# 3s a result" ischemia and necrosis of s(in occurs# Other tissues affected include subcutaneous fat" )isceral organs" and s(eletal muscle# 3 stud b Harima et al reported on the effects of an e)ening snac( in patients recei)ing chemotherap for hepatocellular carcinoma# The reported a lower nonprotein respirator +uotient in patients with ad)anced hepatocellular carcinoma compared with patients with cirrhosis who did not ha)e hepatocellular carcinoma and in patients with earl $stage hepatocellular carcinoma# %atients with cirrhosis and ad)anced hepatocellular carcinoma who were recei)ing chemotherap and who recei)ed the late$e)ening snac( had an impro)ed nonprotein respirator +uotient" branched$chain amino acidBt rosine ratio" alanine aminotransferase le)el" and prealbumin le)el compared with controls#[1@]

"auses
Worldwide" the most common cause of malnutrition is inade+uate food inta(e# %reschool$ aged children in de)eloping countries are often at ris( for malnutrition because of their

dependence on others for food" increased protein and energ re+uirements" immature immune s stems causing a greater susceptibilit to infection" and e0posure to nonh gienic conditions# 3nother significant factor is ineffecti)e weaning secondar to ignorance" poor h giene" economic factors" and cultural factors# The prognosis is worse when protein$energ malnutrition occurs with H4G infection# *astrointestinal infections can and often do precipitate clinical protein$energ malnutrition because of associated diarrhea" anore0ia" )omiting" increased metabolic needs" and decreased intestinal absorption# %arasitic infections pla a ma;or role in man parts of the world# 4n de)eloped countries" inade+uate food inta(e is a less common cause of malnutritionC protein$energ malnutrition is more often caused b decreased absorption or abnormal metabolism# Thus" in de)eloped countries" diseases" such as c stic fibrosis" chronic renal failure" childhood malignancies" congenital heart disease" and neuromuscular diseases" contribute to malnutrition# 1ad diets" inappropriate management of food allergies" and ps chiatric diseases" such as anore0ia ner)osa" can also lead to se)ere protein$energ malnutrition# %opulations in both acute$care and long$term facilities are at ris( for clinicall significant in)oluntar weight loss (4W6) that can result in protein$energ malnutrition# 4W6 is defined as a loss of 8#= (g or greater than =A of the usual bod weight o)er a period of @$ 19 months# %rotein$energ malnutrition occurs when weight loss of greater than 1:A of normal bod weight occurs# &lderl persons often de)elop malnutrition" common causes of which include decreased appetite" dependenc on help for eating" impaired cognition andBor communication" poor positioning" fre+uent acute illnesses with gastrointestinal losses" medications that decrease appetite or increase nutrient losses" pol pharmac " decreased thirst response" decreased abilit to concentrate urine" intentional fluid restriction due to fear of incontinence or cho(ing if d sphagic" ps chosocial factors such as isolation and

depression" monoton of diet" higher nutrient densit re+uirements" and other demands of age" illness" and disease on the bod # &lderl patients are often at ris( for protein$energ malnutrition because of inade+uate nutrition" which has been determined to be a common comorbid factor for increased morbidit and mortalit in elderl burn )ictims#[17] %atients with li)er cirrhosis are also at ris( for protein$energ malnutrition" which is a ris( factor that portends a poor prognosis for sur)i)al# This ris( correlates with the degree of li)er in;ur and the etiolog of li)er in;ur " with the ris( of protein$energ malnutrition being more se)ere in persons with alcoholic cirrhosis than in those with nonalcoholic cirrhosis# %atients on long$term hemodial sis also ma de)elop protein$energ malnutritionC this is associated with increased morbidit and mortalit # %atients with s+uamous cell carcinoma of the esophagus are at ris( for protein$energ malnutrition#

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%rint

Protein-Energy Malnutrition Differential Diagnoses

3uthorK Foah . .cheinfeld" '?" 2?" 133?C /hief &ditorK William ? 2ames" '? more###

O)er)iew %resentation ??0 Wor(up Treatment 1ollow$up

>pdatedK 1eb @" 9:18 Heferences

#i$$erential #iagnoses

3ctinic %rurigo

%roceed to Wor(up

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97# ?e /aprio /" 3lfano 3" .enatore 4" Parrella 6" %asanisi 1" /ontaldo 1# .e)ere acute li)er damage in anore0ia ner)osaK two case reports# Nutrition# 'a 9::@C99(=)K=79$=# ['edline]# 9<# ?elahoussa e 3H" 2orizzo 26# /utaneous manifestations of nutritional disorders# Dermatol #lin# 2ul 1,<,C7(-)K==,$7:# ['edline]# 9,# *laser" D6# %ediatricsK 'alnutrition# 'edstudents# 3)ailable at httpKBBwww#medstudents#com#brBpediaBpedia1#htm# -:# *olden 'HF# .e)ere malnutrition# 4nK Weatherall ?2" 6edingham 2**" Warrell ?3" eds# O&ford !e&tboo' of Medi%ine# -rd ed# 1,,@K197<$,@# -1# *os(owicz '" &ichenfield 61# /utaneous findings of nutritional deficiencies in children# #urr O"in Pediatr# 3ug 1,,-C=(8)K881$=# ['edline]# -9# *upta '3" *upta 3D" Haberman H1# ?ermatologic signs in anore0ia ner)osa and bulimia ner)osa# (r%h Dermatol# Oct 1,<7C19-(1:)K1-<@$,:# ['edline]# --# *urs(i HH" .chirmer //" Hosa 3H" 5rentano 6# Futritional assessment in patients with s+uamous cell carcinoma of the esophagus# He"atogastroenterolog*# Fo)$?ec 9::-C=:(=8)K1,8-$7# ['edline]# -8# Harris /6" 1raser /# 'alnutrition in the institutionalized elderl K the effects on wound healing# Ostom* Wound Manage# Oct 9::8C=:(1:)K=8$@-# ['edline]# -=# Hendric(s D'" ?uggan /" *allagher 6" et al# 'alnutrition in hospitalized pediatric patients# /urrent pre)alence# (r%h Pediatr (doles% Med# Oct 1,,=C18,(1:)K111<$99# ['edline]# -@# 2ilcott .5" 'asso D6" 4c(es .5" ' hre .?" ' hre 23# .ur)i)ing but not +uite thri)ingK anthropometric sur)e of children aged @ to =, months in a rural Western >ganda district# J (m Diet (sso%# Fo) 9::7C1:7(11)K1,<-$<# ['edline]#

-7# Duhl 2" ?a)is '?" Dalaa;i 3F" Damath %." Hand 26" %eine /2# .(in signs as the presenting manifestation of se)ere nutritional deficienc K report of 9 cases# (r%h Dermatol# 'a 9::8C18:(=)K=91$8# ['edline]# -<# 6 der /H# 3ssessing ris( and pre)enting pressure ulcers in patients with cancer# Semin On%ol Nurs# 3ug 9::@C99(-)K17<$<8# ['edline]# -,# 'anguso 1" ?!3mbra *" 'enchise 3" .ollazzo H" ?!3gostino 6# &ffects of an appropriate oral diet on the nutritional status of patients with H/G$related li)er cirrhosisK a prospecti)e stud # #lin Nutr# Oct 9::=C98(=)K7=1$,# ['edline]# 8:# 'c6aren ?.# .(in in protein energ malnutrition# (r%h Dermatol# ?ec 1,<7C19-(19)K1@78$1@7@a# ['edline]# 81# 'iller .2# Futritional deficienc and the s(in# J (m (%ad Dermatol# 2ul 1,<,C91(1)K1$-:# ['edline]# 89# Feldner DH# Futrition" aging and the s(in# Geriatri%s# 1eb 1,<8C-,(9)K@,$<9" <7$ <# ['edline]# 8-# %ell T1" .antillan /1" *ilman HH" et al# Tuberculosis s(in testing" anerg and protein malnutrition in %eru# nt J !uber% Lung Dis# .ep 9::=C,(,)K,77$<8# ['edline]# 88# %rendi)ille 2." 'anfredi 6F# .(in signs of nutritional disorders# Semin Dermatol# 'ar 1,,9C11(1)K<<$,7# ['edline]# 8=# Habinowitz .." *ehri '" .tettler F" ?i %aolo &H# 'arasmus# Meds%a"e )eferen%e [serial online]# 'a 9:" 9::,C3)ailable at httpKBBemedicine#medscape#comBarticleB,<88,@$o)er)iew# 8@# Hoongpisuthipong /" .obhonslidsu( 3" Fantiru; D" .ongchitsomboon .# Futritional assessment in )arious stages of li)er cirrhosis# Nutrition# .ep 9::1C17(,)K7@1$=# ['edline]#

87# H an 3." *oldsmith 63# Futrition and the s(in# #lin Dermatol# 2ul$3ug 1,,@C18(8)K-<,$8:@# ['edline]# 8<# .chneider 25" Forman H3# /utaneous manifestations of endocrine$metabolic disease and nutritional deficienc in the elderl # Dermatol #lin# 2an 9::8C99(1)K9-$-1" )i# ['edline]# 8,# .hah ." Danni(eswaran F" Damat ?# 3 rash# #lin Pediatr +Phila,# .ep 9::7C8@(7)K@=:$8# ['edline]# =:# .hashidhar HH" *rigsb ?*# 'alnutrition# Meds%a"e )eferen%e [serial online]# 3pril ," 9::,C3)ailable at httpKBBemedicine#medscape#comBarticleB,<=18:$ o)er)iew# =1# .oni 5%" 'c6aren ?." .herertz &1# .(in lesions in nutritional" metabolic and heritable disordersK cutaneous changes in nutritional disease# 4nK -itz"atri%'.s Dermatolog* in General Medi%ine# Gol 9# 1,,,K179=$-7# =9# Tirmenta;n$2an(o)ic 5" ?im(o)ic F# [.imple methods for nutritional status assessment in patients treated with repeated hemodial sis]# Med Pregl# .ep$Oct 9::8C=7(,$1:)K8-,$88# ['edline]# =-# Wilmer W3" 'agro /'# /alciph la0isK emerging concepts in pre)ention" diagnosis" and treatment# Semin Dial# 'a $2un 9::9C1=(-)K179$<@# ['edline]# =8# 'a 6" .a)or ." 3gim F*# 3c+uired protein energ malnutrition in glutaric acidemia# Pediatr Dermatol# 2ul$3ug 9:1-C-:(8)K=:9$8# ['edline]# ==# H acinth H4" 3de(e e O3" Oilgwan /.# 'alnutrition in .ic(le /ell 3nemiaK 4mplications for 4nfection" *rowth" and 'aturation# J So% Beha/ Health S%i# 2an 9:1-C1K7(1)# =@# ?orner T&" 6ac(inger /" Haider ." 6uger &" Dapan 3" 6uger '" et al# Futritional inter)ention and ph sical training in malnourished frail communit $dwelling

elderl persons carried out b trained la "buddies"K stud protocol of a randomized controlled trial# BM# Publi% Health# ?ec 9:1-C1-(1)K19-9# ['edline]#

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