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Learned Taste Aversions in Children Receiving Chemotherapy Abstract. Children with neoplastic diseases were offered an unusual ice cream before thelr drag treatments. Patients experiencing gastrointestinal toxicity due 10 the drugs were subsequentty less likely to choose that ice cream again than controls This suggests tha: taste aversions induced by drug-associated symploms may con- tribute to the appetite loss experienced by cancer patients. Garcia and others (1) have demon- stratcd the development of specific taste aversions in a wide variety of animal spe- cies. ln general, these investigators pre- sented a solution to rats prior to adminis- tration of a drug or radíation treatment that presumably induced gastrointestinal (G1) discamfort. “The animals subse- quentiy developed significant aversions to the flavor of the salution, as indicated by their reluctance to ingest il Sub- stantial aversions have been achieved in a single trial; these aversions occur even when there are long intervals (6 to 12 hours) (2) between exposure to the flavor and onset of illness. Therefore, the ac- quisition of laste aversions is a persistent form of learning. To our knowledge there have been no controlled studies of such aversions in humans. Several therapies used in the treatmen: of cancer (certain chemotherapeutic drugs; abdominal ra- diocherapy) are the same as those used to produce conditivned taste aversions in laboratory animals (3). We therefore evaluated patients undergoing such treatments to determine whether similar learned food aversians also occur ín hu- mans. Since cancer patients frequently suler loss of appetile (4), the demonstra- tíon of such aversions would suggest that food aversions may be one factor con- tributing to their anorexia. In the present study we investigate) whether children receiving O! toxic chemotherapy for the treatment of neoplastic disease would acquire aversions fa an unusual ice cream consumaed prior to drug treatment. A total of 41 patients ranging in age from 2 to 16 years participated in the study (5). All wete being treated as out- patients at the Children's Orthopedic Hospital and Medical Center Hematolo- gy Clinic. Patients with advanced or re- fractory disease were excluded. Patients received intravenous doses of chemo- therapeutic drugs, except as noted. Urugs considered significantly toxic to the gastrointestinal tract (GT toxic)—for example, adriamycin, cyclophospham- ide, and cytosine arabinoside—are gen- eradly associated with a moderate to high degree uf nausea or emesis at the doses given patients in this study (6). The onset Of these symptoms may occur a few mn- utes to a few hours after drug administra- tion. Vineristine, a chemotherapeutic agent not associated with these symp- toms, served as a control drug. Patients receiving GT toxic chemother- apy were stratified on the basis of age and number of prior Gl toxic drteg treat- ments and then randomly assigned to one of two groups: the experimental group (group 1) which received a paired association between an unusual ice cream and Gl toxicity: the control group (group 2) which experienced Gl toxicity without recciving any ice cream. Pa- tients receiving chemolherapy not asso- cialed with (11 symptoms (vincristine) or no drug at all, were placed in a second control group (group 3) and seceived the ice cream without experiencing Gl tox- icity (7). During session 1 children in groups land 3 were given 80 g of the novel ice cream, Mapletof (prepared with maple and black walnut favor ex- tracts), 15 10 60 minutes prior Lo their re- ceiving a drug treatment (or for some pi tients im group 3 prior ta a routine check- up). Children in group 2 were not offered ice ercam during session | but were oc- cupied for a comparable amount of time with a tay prior to their drug treatment At this time patients, and thcir parents, in all groups also filled out diet question- naires. Table 1, Choice made by patients during session 2, Toti Patients o number selecting ice cream Treatment in session | of - A Num- Percent- patients Lor pd Group ! Mapletof ice crenm paired with Gi toxicity 14 3 2 Group 2 Gl toxicity alone R 8 e Group 3 Mapletofl ice cream alone 15 "y 17 ON3(+8073/7841616-1302800.50/0 Copyright O 1978 ARAS Fwo to four weeks later (session 2) the acceptance lor rejection) of Mapletoff ice cream was measured by offering children iu all groups a choice between cating the ice ercam or playing with u game. Kesukis (Table 1) indicate that only 21 percent of patients in group 1 chose Mapletoff ice cream during session 2 compared to 67 percent in group 2 and 73 percent in group 3. The difference be- tween the Iwo proportions obtained when the control groups were combined and compared to group 1 was significant le = 3.06, P<= 001). Therefore, Ube consumption of the ice cream before Gl toxic chemotherapy resulted in a lower likelihood of a subsequent choice of that ice cream again than did the G] toxic Therapy alone or the previous sampling of that ice cream without toxic therapy. It could be argued that a choice be tween eating the ¡ce cream and engaging in some other activity is not specific enough to offer evidence of an actual laste aversión, We therefore retested all patients that were still coming to the Hematology Clinic, using a blind proce- dure, by offering them both Mapleto ice cream and another relatively novel ice cream (Hawaiian Delight: Foremost Ice Cream, Seatile, Washington). During these retests patients were asked 10 taste both ice cream flavars, indicate which they preferred, and cat as much of each as they wished. Flavor preference and amount consumed were recorded, Al though these retests occurred an average of 414 months after session |, only 25 percent (3 of 12) of the patients in the ex- perimental group (group 1) said they pre- ferred MapletofF while 66 percent (4 08 6] in group 2 and $0 percent (4 of 8) in group 3 preferred Mapletoff. For each patient a preference measure based ou consump- tion was calculated by determuning the percentage of total ice cream consumed during retest which was Mapletoff. Pref- erence for Mapleto(F ice cream in the ex- perimental group was significantly lower than in the control geonps (8). Total ice cream consumption of the groups did not differ. Thus aversion to the Mapletoff ice eream appears to be a specific, learned Tesponse and nat an effect of the Gl toxic drugs alone, since group 2 palients were not averse to eating the ice cream, Thal the Mapletoff ice cream was not dis tastefal was indicated by the acceptance of il by patients in group 3, who had tasted it before. Therefore, these results demonstrate that humans, like a number of other species, acquire aversions to 4 novel flavor when it is consumed before á treatment which induces Gi) comfort. SCIENCE, VOL, 200, 16 JUNE 1978 Prior experience with drug treatment markedly attenuates the formation of conditioned taste aversions in rats (9). Our results are interesting in that mast of the patients in this study had received many prior treatments thal caused Gl discomfort (the average number per child was 23). Furthermore, most ef the patients were aware that fhe cause of their nausca and vormiting was their ther- apy. These factors, however, did not preciude the formation of long-lasting taste aversions, suggesting that hurans have a strong propensity to form these aversions. Farther data were obtained through the use of questionnaires, the results af which support and extend these findings. Patients completed diet inventory forms during sessions 1 and 2 to provide infar- mation about their food preferences and usual diet, as well as specific foods eaten before drug treatments. These data (/0) revealed that patients receiving Gl tuxic cliemotherapy were significantly more likely to report avoiding or distiking a specific food eaten before a clinic visit than control (group 3) patients. Thus, learned taste aversions may occur not only fo a novel fuod presented by the ex- perimenter just prior to drug administra- tian, but also to foods in fhe patients" dies which happen to be eaten 1p to sey= eral hours before treatment, This is con- sistent with the findings of Gurb and Stunkard (17) that human subjects report the development of aversions to a wide variety of fovds consumed coinciden- tally before a bout of illness. The demonstration of taste aversions in children receiving chemotherapy treatments may prove ta be of impor- tance 1o physicians who sdminister treat- ments which induce nausea and vomst- ing. Such aversions may be one of the factors contributing to the anorexia and weight loss seen in patients with cancer. Additional work is needed to delineate the factors controlting the occurrence of these aversions in order to develop methods for minimizing or eliminating then Trenr L. BERNSTEIA Department of Psychology, University of Washington, and Children's Orthopedic Hospital and Medical Center, Seante 98195 References amd Notes E. García, W. G. Hankins, K. W. Rusiniak, Ser ¿nce 185, 824 (1974); D. Kimoldorí, 1. García, D.0 Robadas, Rudiar, Res. 12, 710 (19680. R- Gustacson, 4. Garcia, W. G, Hankias, KW Kusiniak, Science 184, 581 (197%). C. Johnson. R,_Beaton, K. Hall, Páysiol. Behas, 14, 404 dns, . Garcia, FR Ervin, E. A. Koelling, Psycho nom. Sei: 5, 121 (1968): E. G. Smili and DeL. Roll, ibid, 9. 1111967), 5.13. Revasky,. Comp. Physiol. Psycho. 65, 17 (1968) SCIENCE, YOL.. 200, 16 JUNE 198 3. $. Hl. Revusky and ]. Garcia, in Psychology of Learsirg and Motivacion, G. Bower and 1. 1 Spence, Eds. (Academic Press, New York, 3970), vol. 4, pp, 1-77. G, Costa, Prog. Esp. Tumor Res. 3, 321.(1963)%; Mí. DeWys, Cancer Res, 30, 2816 (1970): S. D: Marrison, Physiol. Eehaw. X7, 705 (1976). ib diagoses sí Ive pgs lis study were sroup_L limphoma 18. Iynsphosarcoma O). acute Iymphoeytis Teukema (2), acute myclog" enous leukemia (2), Wilms tartar (3), Ewings sarcama (1), Hodgkins disease (1): grnuy 2: Iymm- phoma (1, acute hymphocyie jeskemia (2), VWilms tomor (1), Ewvings sarcoma (1), Hodgións «israse (1), osteogenic sarcoma (1). rhabdosar- coma (1). “otiosarcoma (1). astrosarcama (1): group 3: acute Iymphocytis leukemia (10), ideo" puthic tbrombosytopenia (3), astzocyloma (ll, undiferentiated leukemia £1). L. . Goodman and A. Gilma togical Basis of Therapeuties (Macmillan, New Yi, ed. 5, 19), pp. 1254-1307. Patiits do ¡nous Y and 2 reneived Tolluwing doses ol chemothermpen known 10 cause significant GI discomfort: (men bers ín parentheses indicate the number Of pa- bits m geovos 1 and. cesrecively, ceceviag Iriamycio, 20 1n 80 mglar 12, 4) daanomycia, 48 10/40 mr (0, yu phos: phamide, 500 10 1200 mglm" (5, Dx eytotine árabinoside, 100 ro 180 img? Cl, 2) acti momycin D. 316 agia (1, 0); trogen mustard, 6 mgira" (0, 1): procarbazive, 190 ragjen? orally (1, O).or a combination ol Gl toxic drugs: adciamy" . 20.10 40 mg/m, plos cytasine aratinosido, The Pharmaco= O method for ex wos developed! was > suppressed by inversidy Jemalos are eliminated when During un experiment conduct Salvador, Lofgren er al male method for the control of Anop eles albimanus, an important vector o] development of this alternat method is most desirable an ate at this time, The successgff the sterile male method relies on theÁficient distri- bution af inundative pfeascs al com- petitive, sterile malgPinto the natural habitat of the target hecios. Therefore, a sound system mu be available for the mass productigf of sterile males, but since the fenules of anopheline species malaria vectors, they he egg or sarly larval stages, the production of males could be con- 1cd less expensively, 0036-907577 netic Method for the Preferential Elimination of 110S16-1305500.50/0. Copyright £: 1978 AMAS. 100 men (3, 1); Saza cytidine, 100 mgfa, plus eponie abia, 2% mL. Os o »pbamide, 300 mg, plus adramycia, 60 gral, 1); eyclorhasphmido: 300 mg”, plus Situorvuracil, 225 mglen (D, 1). In addition to he G] toxic drugs, 9 of 14 patients in growp 1 and 6 of 12 patients in group 2 received antiemetios; 6 of 14 patients in group | and $ ur 22 patients a group 2 received vineristine (1.5 mgla*). Re- Ports ol nuusea or emesjs, or both, ranging from mild to severe vecurred in 11 of 14 patients 11 group t and 8 012 pulents ia group 2. ln gronp 3. 11 patients received vineristine (1.20 2.0 mg m3), 4 patients received no drug treatment. There were no reports af nausca or emesis 10 Us gloup. A signilicanly lower percentage of the ice crear consumed by ¿roup 1 lexperimental) patients was Mapleto8 as compared ln the Combined crol Mana ines Ue s Re L. Elkins, Physiol. Payekol. 2, 34] (1974); 4. 1 Gaudie, M. Taylor, H. Atherton, Pharmacol. Biockem. Rehav. 3, 947 11975), 10: Y Lo Beresteia in erre TL Cart and A. ). Stunkard, Am. 3. Psychia- PO, 12, Y thank M, 1. Wallece, J. Haccmano, 1. D, Bern- stejn, R, Chara, and W. A. Bleyer fos invaluable sssistange in 1he implecuentation of this sludy Supported by the Diet, Nutrition, and Cancer Program af the Natiamal Cancer Instilute (CP 65790-68). 1 also thank R. Rolles and S. Woods Tor Iber critical reading of the menusenpt 16 December 1977 És no practical generic method Broxwphenyl methyl> (Y:2R) transtocation, ination ot A. albimanas females in a ss production process are only 85 to 95 percent effective (unpublised data), we undertook the development of a ge- tic method for the preferential killing ol emales. We now describe (he syn- etic sexing scheme utilizes propoxur W-isopropoxyphenyl methyl- carbamate) Mgcentibility (pr!) as n reces- sive conditionAkethal, a V(Y :2R) trans- location, and ana2R) inversion. The locus for propoxuk resistance (pr), a dominant trait, is ON,the right arm of chromosome 2, and thiBkgllele was linked to the Y chromosome vidky radiation-in- duced translocation, Adullomozygous resistant males (prí/pr), than 24 hours old, were irradiated with ¿700 R (dose rate 212 R/min) from an x-Phy ru chine operated at 90 kY (peak), The! radiated males were crossed to suscdp- 1 
