Cows' milk sensitive enteropathy in cystic fibrosis
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- Phebe Randall
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1 Archives of Disese in Childhood, 1989, 64, Cows' milk sensitive enteropthy in cystic fibrosis S M HILL, A D PHILLIPS, M MEARNS, AND J A WALKER-SMITH Acdemic Deprtment of Child Helth, Queen Elizbeth Hospitl for Children, London SUMMARY Proximl smll intestinl mucosl biopsies were crried out in children with cystic fibrosis who hd dirrhoe nd filed to thrive in spite of dequte tretment, including pncretic supplements. Histologicl exmintion of eight of the 17 biopsies tken over period of 12 yers showed evidence of enteropthy, nd ccounted for one in 13 (8%) children with cystic fibrosis under 3 yers of ge ttending our clinic. Seven responded to cows' milk free diet; the dirrhoe stopped nd weight gin incresed. One of these responded only when gluten ws lso excluded from his diet. The eighth child remined on norml diet nd his symptoms did not improve. The enteropthy hd resolved in ll five ptients who hd further biopsies tken while receiving tretment, nd from 15 months to 3 yers of ge ll the children tolerted norml diet nd continued to thrive. Cows' milk sensitive enteropthy is n importnt cuse of filure to thrive in children with cystic fibrosis. Smll intestinl biopsy is n importnt investigtion in younger children who fil to thrive nd hve dirrhoe despite dequte tretment. Children with cystic fibrosis often fil to thrive. This filure is usully relted to the disese itself, nd my be the result of recurrent chest infections, indequte food, or pncretic enzyme deficiency. Two gstrointestinl diseses tht my, in ssocition with cystic fibrosis, cuse filure to thrive re coelic disese1 2 nd lctse deficiency.3 4 It is importnt to mke the correct dignosis when child with cystic fibrosis is filing to thrive s the severity of the respirtory component of the disese (which my ffect prognosis) seems to be relted to the child's nutritionl stte. The im of this study ws to investigte whether cows' milk sensitive enteropthy is cuse of chronic dirrhoe nd filure to thrive in children with cystic fibrosis. tking no mediction t the time of biopsy. The weights of ll the children were below the 25th percentile, nd five were well below the third. Nine of the children were boys nd eight girls. They were ged from 3 months to 12 yers (medin 12 months). In ll cses the dignosis of cystic fibrosis ws mde from two positive swet tests nd typicl symptoms. Swet tests were considered positive if t lest 1 mg of swet ws collected tht contined t lest 7 mmol/i sodium. The dignosis of cows' milk sensitive enteropthy ws mde when chrcteristic histologicl findings were present in proximl smll intestinl mucosl biopsy specimen, nd there ws rpid clinicl response to the exclusion of cows' milk from the diet.7 Erly chllenge with cows' milk nd further Ptients nd methods smll intestinl biopsies were necessry to prove tht the disese ws present. In prctice, s the Seventeen children were included in the study from condition ws temporry one nd there ws risk Fifteen of the ptients were lredy of nphylxis on the reintroduction of cows' milk, ttending the cystic fibrosis clinic nd were selected chllenge ws not considered necessry if the for smll intestinl mucosl biopsy becuse they histology ws chrcteristic nd the clinicl improvement rpid. were filing to thrive in spite of dequte tretment for cystic fibrosis. This included pncretic enzyme At the time of smll intestinl mucosl biopsy, 16 nd ft soluble vitmin supplements. Two other of the children were on cows' milk bsed feeds, nd children underwent smll intestinl mucosl biopsy one ws brest fed. The mother of the ltter child nd swet tests during the sme dmission s prt of included cows' milk in her diet. Three children the routine procedure for investigtion of filure to under 6 months old were on full ft dpted formul thrive, nd hd positive swet tests. They were feeds, three were tking 'cystic mix' (SMA nd 1251 Arch Dis Child: first published s /dc on 1 September Downloded from on 2 October 218 by guest. Protected by
2 1252 Hill, Phillips, Merns, nd Wlker-Smith Mrvel with dded Cloreen), nd the other 1 were hving skimmed milk. The 13 oldest children included norml mount of gluten in their diets, but the four youngest hd not strted solids. Stool smples were tken from ll ptients nd exmined for pthogens. The smll intestinl mucosl biospy specimens were tken fter full informed consent hd been given by the prents. After n overnight fst, peditric sized double port cpsule ws used to obtin mucos from the duodenojejunl flexure under rdiologicl control. In ddition to the biopsy specimen, duodenl juice ws spirted if possible nd exmined for the presence of Girdi lmbli. A smple of tissue from one biopsy specimen from ech ptient ws frozen in liquid nitrogen nd used to ssy discchridses,8 nd the other ws fixed in forml sline nd processed for histologicl exmintion. Suitble specimens were lso nlysed morphometriclly using computer bsed imge nlysis system.6 If the histologicl ppernce of biopsy ws bnorml nd consistent with cows' milk sensitive enteropthy6 the child ws given cows' milk exclusion diet for the next few months, usully until t lest 15 to 18 months of ge. These children were reviewed regulrly in the outptient clinic with prticulr ttention being pid to weight gin nd stool frequency. If possible proximl smll intestinl mucosl biopsy ws repeted before cows' milk ws reintroduced to their diets. Morphometric nlysis of the biopsy specimens ws gin performed nd the results were compred with those of the specimens obtined on presenttion. Other fetures of the children with enteropthies tht were reviewed were: the mnner of initil presenttion with cystic fibrosis; personl or fmily history of topy; nd ny investigtions which might hve indicted n topic tendency. These included exmintion of peripherl blood for eosinophils, skin prick tests for llergens, nd estimtion of serum IgE nd specific IgE concentrtions. Sixteen per cent of ll children ttending our clinic during the 12 yer period presented with meconium ileus. Results In nine of the 17 children proximl smll intestinl biopsy specimens were histologiclly norml. They were ged from 3 months to 12 yers (medin 2 yers). Seven were girls nd two boys. No pthogenic orgnisms were detected in their stool smples, nd G lmbli ws not detected in ny duodenl spirte. No gstrointestinl cuse other thn cystic fibrosis ws found to explin their filure to thrive nd chronic dirrhoe. Histologicl nd morphometric findings in the biopsy specimens from the remining eight children were bnorml nd consistent with cows' milk sensitive enteropthy-tht is, they hd thin mucos with reduced villous height (fig 1). Seven of these children were boys, nd their ges rnged from 5 months to 28 months (medin 1). This group included one of the children who underwent smll intestinl mucosl biopsy t the sme time s cystic fibrosis ws dignosed. Rotvirus ws detected by electron microscopy both in the stool nd within the smll intestinl mucos of one child. No pthogens were detected in stool or duodenl spirte from ny other ptient. The child with most frequent dirrhoe (1 times dy) hd n enteropthy, while the child without dirrhoe did not. Aprt from these two cses, there ws no obvious difference in stool output between those children with enteropthy nd those with norml smll intestinl mucos. Ptients with enteropthy were on vriety of cows' milk bsed feeds. Three were on formul feeds, two were on cystic mix, one ws on doorstep milk, nd the other two on skimmed milk. Four of the eight children with enteropthy hd originlly presented with meconium ileus, wheres bout 16% of ll children ttending the clinic over the 12 yers hd presented in this mnner. The other four hd presented with filure to thrive, nd one lso hd recurrent chest infections. At the time of smll intestinl mucosl biopsy the weights of five were below the third percentile (nd the other three on or below the 1th), ll their birth weights hd o 3. CL., >U -C - I c u} *O1-~~~~~~~ -7-6 c 3 U, -5 -.~~~~~~~~~~~ U' : I -4 -n 3F [lj ị ~.... -UU.JVV U-- Norml Ptients with Norml Ptients with subjects enteropthy subjects enteropthy Fig 1 Morphometric findings in ptients with nd without cows' milk sensitive enteropthy. Dots represent the 13 ptients studied, nd verticl brs the findings ofmluend etl (men (SD)).6 oh Arch Dis Child: first published s /dc on 1 September Downloded from on 2 October 218 by guest. Protected by
3 been in the norml rnge. All seven vilble for follow up hd developed topic symptoms, which included sthm in five, eczem in two, nd urticri in one. Three children hd pprecible eosinophili (more thn 4x 16/1) on t lest one occsion. Discchridse ctivities were norml in the four histologiclly norml biopsy specimens in which they were mesured. Sucrse nd mltse ctivities were norml in the six children with enteropthy in which they were mesured. Lctse ctivity ws reduced in two (-5 nd -8 mmol/min/g). This ws not ssocited with clinicl lctose intolernce in either child. Seven of the eight children with smll bowel mucosl bnormlities comptible with the dignosis of cows' milk sensitive enteropthy hd cows' milk withdrwn from their diets; Pregestimil ws used s substitute feed. The dignosis does not seem to hve been considered in one child who ws biopsied in 1976, who remined on cows' milk, nd who continued to fil to thrive. He died from chest infection ged 3 yers. In six of the seven children stool consistency improved, stool frequency fell to two or three times dy, nd they hd 'ctch up' weight gin. One child whose weight on presenttion ws well below the third percentile (3.6 kg t 6 months) lmost reched this percentile in six months. One child's weight climbed from the third to the 1th percentile, two from the tenth to the 25th, nd two reched the 5th percentile (one from the third nd the other from the 1th). The one child who did not improve rpidly underwent further proximl smll intestinl biopsy, which showed tht enteropthy ws still present. Gluten ws excluded from his diet in ddition to cows' milk, nd third biopsy showed improvement in the histologicl picture. He underwent two further biopsies, both of which were norml. The first ws t 3 yers of ge fter cows' milk ws reintroduced to his diet, nd the other t 4 yers of ge when his diet lso included gluten, so he hd trnsient gluten intolernce rther thn coelic disese. Smll intestinl biopsy ws lso repeted in four of the seven other children with enteropthy 2-14 months lter while they were receiving cows' milk free diets. Resons for not repeting the biopsy in the other three were: dverse socil circumstnces (n=1), follow up continued elsewhere (n=1), nd cows' milk sensitive enteropthy not recognised (n=1). All five biopsy specimens showed obvious improvement on histologicl exmintion. Four of the five specimens were suitble for morphometric nlysis. Fig 2 shows the results of morphometry in these, nd compres them with the Cows' milk sensitive enteropthy in cystic fibrosis 1253 '. 2 z l 2- c N c 1._ 'C ZU. -J. I I I I P 3 C -5 _ n -4 WI =3 UV L 3U Ptients t Ptients on Ptients t Ptients on presenttion diet free of presenttion diet free of cows' milk cows' milk Morphometric findings in ptients with cows' milk Fig 2 sensitive enteropthy on presenttion nd on dietfree of cows' milk. Dots represent thefour ptients biopsied twice, nd verticl brs thefindings ofmluend et l (men (SD)).6 morphometric findings on presenttion. In four the mucosl thickness improved, nd in ll cses the rtio of villous height:crypt zone depth improved. Discchridse ctivities were gin mesured, nd the child who hd hd the lowest lctse ctivity now hd one within the norml rnge (1.8). The children were chllenged with cows' milk from 2-13 months (medin 1 months) fter excluding it from their diets. There were no dverse rections, weight gin continued t the sme rte s previously, nd stool frequency ws unchnged. Discussion ---4 Cows' milk sensitive enteropthy ws common problem mong the children under 3 yers old (8/13, 62%) who were selected from our cystic fibrosis clinic for smll intestinl mucosl biopsy. As 15 children hd presented to our clinic by 3 yers of ge from , the overll incidence of the enteropthy in children presenting with cystic fibrosis in this ge group ws 1/13. The incidence of cows' milk sensitive enteropthy in the generl popultion is difficult to estblish, prticulrly s so mny children re strted on restricted diets without seeing doctor, but it seems to be considerbly lower thn this.9 Three possible resons for high incidence in children with cystic fibrosis re: the ssocition of cystic fibrosis with topy' (cows' milk sensitive enteropthy is n topic relted disorder), incresed intestinl permebility,1' nd impired digestion of protein due to insufficient pncretic trypsin leding to high ntigen lod presenting to the smll intestinl mucos. 'C Arch Dis Child: first published s /dc on 1 September Downloded from on 2 October 218 by guest. Protected by
4 1254 Hill, Phillips, Merns, nd Wlker-Smith The min fetures of this group of ptients were the unequl sex rtio, the high incidence of topy, nd the presenttion with meconium ileus. A predominence of boys with fmily history of topy hs previously been reported in group of children presenting with cows' milk sensitivity.12 Atopic symptoms re common in children with cows' milk sensitive enteropthy lone,13 nd s lredy mentioned topy is ssocited with cystic fibrosis.1 The incidence of meconium ileus would of course be higher in this group thn mong ll children with cystic fibrosis, s cows' milk sensitive enteropthy is disese of infncy, nd mny children with cystic fibrosis present lter. The incidence of 5% is surprisingly high, however, when the overll incidence in our clinic ws 16%. In some cses, lthough the mucosl ppernce hd improved when cows' milk ws excluded from the diet, it ws not entirely norml. This is similr to previous findings6 nd could indicte tht in spite of dvice from dietitin these children my hve continued to ingest some cows' milk. Alterntively they my hve rected to Pregestimil or other dietry constituents, lthough this ws not cliniclly pprent. One child ws intolernt of gluten, which illustrtes the fct tht multiple food intolernces my co-exist. 14 It ws becuse of this tht Pregestimil ws used s cows' milk substitute (rther thn soy bsed milk), becuse t lest 15% of children intolernt of cows' milk lso rect to soy milk.7 As ll the children treted for cows' milk sensitive enteropthy were given Pregestimil feeds, there were no 'control' children. It could be rgued tht children with cystic fibrosis, even without cows' milk sensitive enteropthy, would thrive better on Pregestimil thn cows' milk feeds becuse Pregestimil contins ft in the form of medium chin triglycerides which re wter miscible nd more rpidly hydrolysed by pncretic lipse thn long chin triglycerides. Cows' milk feeds, however, do hve the dvntges of higher slt nd protein contents. When our group of children were restrted on diets contining cows' milk there were no noticeble chnges in the rte of weight gin, so there ws no evidence tht either milk ws superior once tolernce to cows' milk hd been chieved. Although cses of cows' milk sensitive enteropthy in ptients with cystic fibrosis do not seem to hve been reported previously, the enteropthy my hve been described Antonowicz et l reported 27 cses of cystic fibrosis with stetorrhoe in ssocition with smll bowel enteropthy; no explntion for the enteropthies ws given.4 Reduction in discchridse ctivities ws thought to be secondry to the prtil villous trophy (s in our two cses with low ctivities of lctse on presenttion). Nordio et l lso described child with reduced discchridses 'ssocited with fltness of intestinl mucos'.'5 Of 17 children with cystic fibrosis described by Gibbons, the one ptient with clinicl nd biochemicl evidence of lctse intolernce underwent smll intestinl biopsy.'6 There ws flttening of the mucos with villous trophy nd reduced discchridse ctivity. No explntion ws given for the enteropthy. In view of our findings, it seems likely tht some of these cses were of cows' milk sensitive enteropthy. Only two of our children hd low lctse ctivity on presenttion, nd there ws no evidence of lctose intolernce. Lctse deficiency hs been ssocited with cystic fibrosis in the pst There ws single cse report of lctse deficiency in 3 yer old boy in 1963,3 nd three cses were reported in In 1968 seven cses were described4 nd genetic ssocition with cystic fibrosis ws postulted, but on review 1 yers lter17 the incidence ws considered to be no higher thn in the generl popultion nd ws thus thought not to be secondry to cystic fibrosis. Other reports hve been indequte s either the dignosis of cystic fibrosis ws in doubt s swet tests were norml,'8 or lctose lod did not cuse dirrhoe. 16 In conclusion, cows' milk sensitive enteropthy should be considered in the differentil dignosis of persistent filure to thrive in younger children with cystic fibrosis, prticulrly in view of our high incidence of 1/13 in ptients under 3 yers of ge. We would not recommend cows' milk free diet for newly dignosed infnts with cystic fibrosis if they re gining weight well nd hve formed stools on tretment with pncretic supplements, but there my be plce for giving medium chin triglyceride contining protein hydrolyste formul feed plus pncretic supplements to newly dignosed infnts who hve frequent stools nd poor weight gin on tretment with suitble cows' milk bsed feed nd pncretic supplements. Some clinicins, however, might prefer to do smll intestinl biopsy first to exclude the rre cse of coelic disese. It is importnt to mke the dignosis nd tret correctly s optiml nutritionl stte is thought to hve such profound effect on overll helth, nd possibly survivl.19 2 Recurrent respirtory infections, which cn result in reduced life expectncy, re thought to be less of problem in child in good nutritionl stte,5 nd this study shows tht cows' milk elimintion hs n pprecible impct on the nutritionl stte of some ptients with cystic fibrosis. References ' Anderson DH. Cystic fibrosis of the pncres nd its reltion to Arch Dis Child: first published s /dc on 1 September Downloded from on 2 October 218 by guest. Protected by
5 coelic disese. A clinicl pthology study. Am J Dis Child 1938;56: Tylor B, Sokol G. Cystic fibrosis nd coelic disese: report of two cses. Arch Dis Child 1973;48: Cozetto FJ. Intestinl lctse deficiency in ptient with cystic fibrosis: report of cse with enzyme ssy. Peditrics 1963;32: Antonowicz I, Reddy V, Khw KT, Shwchmn H. Lctse deficiency in ptients with cystic fibrosis. J Peditr 1968;42: Shepprd R, Cooksley WGE, Cook WDD. Improved growth nd clinicl nutrition nd respirtory chnges in response to nutritionl therpy in cystic fibrosis. J Peditr 198;97: Mluend C, Phillips AD, Briddon A, Wlker-Smith JA. Quntittive nlysis of smll intestinl mucos in cows' milk sensitive enteropthy. J Peditr Gstroenterol Nutr 1984;3: Wlker-Smith JA. Milk intolernce in children. Clin Allergy 1986;16: Phillips AD, Avigd S, Scks J, Rice SJ, Wlker-Smith JA. Microvillous surfce re in secondry discchridse deficiency. Gut 198;21: Ron RJ, Chinn S. Prents' perception of food intolernce in primry school children. Br Med J 1987;294: Hodson ME, Wrner JO. Immunology. In: Hodson ME, Normn AP, Btten JC, eds. Cystic fibrosis. London: Blliere Tindll, 1983:91-6. Leclercq-Foucrt J, Forget PP, Vn Cutsem JL. Lctuloserhmnose intestinl permebility in children with cystic fibrosis. J Peditr Gstroenterol Nutr 1987;6: Hlpem SR, Sellrs WA, Johnson RB, Anderson DW, Spenstein S, Reisch JS. Development of llergy in children fed Cows' milk sensitive enteropthy in cystic fibrosis 1255 brest, soy or cows' milk in the first six months of life. J Allergy Clin Immunol 1973;51: Digeon B, Wlker-Smith JA. Food intolernce nd gstrointestinl disese in infncy: personl prctice. Dig Dis 1986;4: Vitori JC, Cmrero C, Cojo A, Ruiz A, Rodrigukez-Sorino J. Enteropthy relted to fish, rice nd chicken. Arch Dis Child 1982;57: Nordio S, Lmedic GM, Beno A, Vignolo L. Discchridse ctivities of duodenl mucos in children. Ann Peditr 1966;26: Gibbons ISE. Discchridses nd cystic fibrosis of the pncres. Arch Dis Child 1969;44: Antonowicz I, Lebenthl E, Shwchmn H. Discchridse ctivities in smll intestinl mucos in ptients with cystic fibrosis. J Peditr 1978;92: Jones RHT. Discchride intolernce nd mucoviscidosis. Lncet 1964;ii: Goodchild M. Prcticl mngement of nutrition nd gstrointestinl trct in cystic fibrosis. J R Soc Med 1986;79(suppl 12): Levy LD, Durie PR, Penchrz PB, Corey L. Effects of longterm nutritionl rehbilittion on body composition nd clinicl sttus in mlnourished children nd dolescents with cystic fibrosis. J Peditr 1985;17: Correspondence to Dr SM Hill, Deprtment of Child Helth, Institute of Child Helth, 3 Guilford Street, London WC1N 1EH. Accepted 8 Mrch 1989 Arch Dis Child: first published s /dc on 1 September Downloded from on 2 October 218 by guest. Protected by
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