THE JOURNAL OF ALTERNATIVE AND COMPLEMENTARY MEDICINE Volume 15, Number 7, 2009, pp.

787792 Mary Ann Liebert, Inc. DOI: 10.1089=acm.2008.0467

The Use and the User of Herbal Remedies During Pregnancy

Lone Holst, M.Sc.Pharm.,1 David Wright, Ph.D.,2 Svein Haavik, Ph.D.,3 and Hedvig Nordeng, Ph.D.4

Abstract

Background: The physiologic changes that occur during pregnancy can lead to a variety of conditions that can usually be self-treated. There are no licensed medicines for conditions such as morning sickness or insomnia in pregnancy, and evidence from Western countries suggests that patients often resort to using herbal medicines. Research on the health behaviors of pregnant women in the United Kingdom with respect to herbal remedies has not been undertaken. Objective: The objective of this study is to describe the use and the user of herbal remedies during pregnancy and to study the sources of information about herbs used. Design: The study design was a survey among expectant mothers more than 20 weeks pregnant presenting at an antenatal clinic. Setting: The setting was an antenatal clinic and antenatal ultrasound department at Norfolk and Norwich University Hospital. One thousand and thirty-seven (1037) questionnaires were handed out between November 2007 and February 2008. Results: Five hundred and seventy-eight (578) questionnaires were returned (55.7%). Three hundred and thirtyfour (334) of the 578 respondents (57.8%) reported using herbal remedies during pregnancy with a mean of 1.2 remedies per woman (median: 1, range: 010). The most commonly used remedies were ginger, cranberry, and raspberry leaf. The most probable user had been pregnant before and had a university degree. Family and friends were the most frequently cited source of information about herbal remedies during pregnancy, and more than 75% of the users reportedly did not tell their doctor or midwife about the use. Conclusions: A large percentage of the women in the study used herbal remedies during pregnancymany of them without informing their doctor or midwife. Doctors or midwives should ask pregnant women if they use herbal remedies during pregnancy. Health care personnel should be open to discuss the use of herbal remedies during pregnancy and be able to give balanced information as the use is so widespread.

Introduction he numerous physiologic changes that occur during pregnancy commonly result in a variety of conditions including morning sickness (70%1), insomnia (66%94%2), heartburn (3050%3), constipation (11%38%4), ankle edema (12%5), anemia (14%52% in third trimester6), and urinary tract infection (1%13%7), among others. Licensed overthe-counter medicines are only available for a limited number of conditions associated with pregnancy, and this may be one factor that leads women to choose alternative remedies. It is suggested that concerns by women regarding use of pharmaceuticals in pregnancy can make people more interested in
1 2

seeking perceived safer alternatives such as herbal remedies.814 Although authors regularly make this assertion, the relationship between negative attitudes to conventional medicines in pregnancy and use of alternative therapies has not been quantied.9,10,13 The lack of license status for conventional medicines in pregnancy, however, is frequently not due to safety reasons but rather to unwillingness to test products in this patient group. Therefore, there are conventional medicines that have been widely used and monitored in pregnancy with no evidence of adverse effects (e.g., prochlorperazine15), and these are prescribed when the prescriber perceives that the benets outweigh the risks. Interestingly, however, evidence seems

Department of Chemistry=Centre for Pharmacy, University of Bergen, Bergen, Norway. School of Chemical Sciences and Pharmacy, University of East Anglia, England. 3 Centre for Pharmacy, University of Bergen, Norway. 4 School of Pharmacy, University of Oslo, Norway.

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788 to suggest that pregnant women frequently seek and utilize herbal remedies8 in preference to Western medicines, which are monitored when used for unlicensed purposes, such as pregnancy. In the United States, use of herbal remedies in pregnancy is believed to range from 4% to 45%,9,13,1618 in Australia it is between 12% and 62%,12,1921 and in Canada between 61 and 96%.8,14 One (1) Norwegian study found that 36% of pregnant women reported using herbal remedies.10 Certain characteristics are more predictive of herbal remedy use and these include older, tertiary educated, English-speaking, nonsmokers, and primiparous.19 Gibson (United States)16 reported that trends were seen toward greater use among white women and women with at least college education but no association to age or income level. Hepner (United States) reported that the use of herbal remedies was most frequent in the age group 4150 years, but that the difference was not signicant.9 Maats (Australia) reported that women using herbs were more likely to be primiparous, married, and to have a tertiary level of education.21 Nordeng (Norway) reported that women between 26 and 35 years of age, with a prior history of use and with higher knowledge about herbs, were more prone to use herbs during pregnancy.22 Refuerzo (United States) found signicantly higher use of herbal treatments among older women of higher socioeconomic class and with higher education.18 There is no complete agreement among the authors, but age and education seem to be the most important factors. No similar studies are found about the use of herbs during pregnancy in the United Kingdom. Also, no research in the United Kingdom has been undertaken to determine the actual and preferred sources of information on herbal drugs. The aims of the study were to describe the use and the user of herbal remedies during pregnancy and to explore the health-seeking behavior of users and nonusers of herbal remedies during pregnancy. Materials and Methods The questionnaire The survey was based on a questionnaire developed by Nordeng10 at the University of Oslo, Norway. To clarify what kind of remedies the study was concerned about, the following denition of an herbal preparation or medicine was given in the questionnaire: any kind of product, such as a tablet, a mixture, an ointment or herbal teas which are produced from plants and used to acquire better health. The following sociodemographic and lifestyle data were collected: Year of birth, number of pregnancies prior to this one, marital status, smoking during pregnancy, medicines taken regularly, education level, and payment for prescription medicines (as a proxy for social status). Prior use of herbal remedies was ascertained and specic questions regarding nine different herbal remedies were included (Table 1). For each remedy, participants were asked if they were aware of it and if so, whether they had used it during pregnancy and if so, what condition they had used it for. An open question about other herbal remedies used was also included. Participants who had used herbal remedies were asked about who recommended it to them and if they had told their doctor about the use.

HOLST ET AL. Table 1. The Nine Different Herbs for Which Specic Questions were Asked Common name Echinacea, coneower Floradix Ginger Chamomile Valerian Cranberry Horsetail Raspberry leaf St. Johns wort Latin (binomial) name Echinacea purpurea (L.) Monech, Echinacea angustifolia DC, Echinacea pallida (Nutt.) Mixture of iron-rich herbs Zingiber ofcinale Roscoe Matricaria recutita L. Valeriana ofcinalis L. Vaccinium macrocarpon Aiton Equisetum arvense L. Rubus idaeus L. Hypericum perforatum L.

Study population and data collection Expectant mothers more than 20 weeks pregnant presenting at the antenatal clinics held within Norfolk and Norwich University Hospital (NNUH) teaching hospital between November 26, 2007 and February 15, 2008 were given a patient information leaet, a questionnaire, and a stamped addressed envelope. The envelope was handed out by the researcher in the waiting room while the women were waiting to go to their appointment. The researcher explained the aim of the study for each potential participant. Statistics Chi-square tests were used to analyse univariate associations between variables. Logistic regression was used to study associations between sociodemographic and lifestyle variables and use of herbal remedies during pregnancy. Forward logistic regression analysis was used to generate models. Variables related to use of herbal remedies with signicance level of 0.05 or greater were included in the model. Interaction factors were included in addition to single variables where appropriate. The statistical analyses were performed using Statistical Packages for Social Sciences (SPSS) version 15. Ethics The study was approved by the Essex 1 Research Ethics Committee, Harlow, Essex, UK. Results The user and the use of herbal remedies during pregnancy Altogether, 1037 questionnaires were given to women more than 20 weeks pregnant presenting at the antenatal clinics held within NNUH teaching hospital. Of those, 578 were returned (55.7%). Three hundred and thirty-four (334) of the 578 women (57.8%) had used herbal remedies during pregnancy with a mean of 1.2 remedies per woman (median: 1, range: 010). Characteristics of the participants are given in Table 2. Most of the women (363 corresponding to 62.8%) had been pregnant before. Almost all women were married or cohabitant (514 corresponding to 88.9%). Approximately equal amounts had General Certicate of Secondary Education (GCSE)=Ordinary-level (O-level) (32.2%) and university

USE OF HERBAL REMEDIES IN PREGNANCY Table 2. Characteristics of the 578 Women in the Study According to Use of Herbal Remedies During Pregnancy Characteristics Total (%) Used herbs before No Uncertain Yes Age (years) 30 >30 Prior pregnancies None 1 or more Smoking during pregnancy Not at all Now and then Daily Marital status Married=cohabitant Single Other Highest completed education GCSE=O-level A-level or other lower education University degree Medicines taken regularly No Yes Pay for prescriptionsb No Yes 578 (100.0) 182 (31.5) 30 (5.2) 357 (61.8) 249 (43.1) 310 (53.6) 197 (34.1) 362 (62.6) 478 (82.7) 55 (9.5) 29 (5.0) 514 (88.9) 39 (6.7) 11 (1.9) 186 (32.2) 179 (31.0) 183 (31.7) 447 (77.3) 109 (18.9) 267 (46.2) 291 (50.3) Users of herbs during pregnancy 334 (57.8) 53 (15.9) 12 (3.6) 262a (79.4) 112 (33.5) 198a (59.3) 101 (30.2) 225a (67.4) 277 (82.9) 35 (10.5) 17 (5.1) 304 (91.0) 22 (6.6) 4 (1.2) 98 (29.3) 97 (29.0) 127a (38.0) 255 (76.3) 71 (21.3) 150 (44.9) 178a (53.3)

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Nonusers of herbs during pregnancy 244 (42.2) 129 (52.9) 18 (7.4) 95 (38.9) 118 (48.4) 131 (46.3) 96 (39.3) 137 (56.1) 201 (82.3) 20 (8.2) 12 (4.9) 210 (86.1) 17 (7.0) 7 (2.9) 88 (36.1) 82 (33.6) 56 (23.0) 192 (78.7) 38 (15.6) 117 (48.0) 113 (46.3)

Sums do not always add up due to missing information. GCSE, General Certicate of Secondary Education, O-level, Ordinary level. a Statistically signicant difference. b Might not give a completely correct picture as pregnant women do not pay for prescription medicines.

education (31.7%). Signicantly ( p < 0.05) more women who had used herbs in the past also used them during pregnancy. The variables tested in the logistic regression were: age, education, number of prior pregnancies, and pay for prescriptions and all interaction factors among those. The only signicant factor was the interaction between number of prior pregnancies and education, Exp (B) 3.245 (1.992; 5.288), Wald 22.337 ( p < 0.05). The Hosmer-Lemeshow goodness-of-t test showed a p 1.0, which supports the model. The most probable user had a university degree and had been pregnant before. The most commonly used herbs in pregnancy are presented in Table 3. It is seen that the six most commonly used were among the ones asked specically about. The remaining three of those had hardly any users (valerian: 4, St. Johns wort: 2, and horsetail: 1). Another 28 remedies were mentioned by users but none of them had more than 5 users. In addition, 15 participants reported use of homeopathic remedies, but they are not included in the analysis. Information-seeking behavior of users and nonusers of herbal remedies during pregnancy The sources of information about herbs used during pregnancy are given in Table 4.

Family and friends were reported to be the most used source of information about herbs taken during pregnancy. Information from health care personnel (doctor, midwife, nurse, pharmacist) was received by 71 (21.3%) of the users. Only 5.8% of the users got their information from an alternative practitioner. Of the 262 women who answered the question about informing their doctor about use of herbal remedies, 200 (76.3%) did not, 18 (6.9%) were uncertain, and 44 (16.8%) did. Preferred sources of information for future questions about herbs are given in Table 5. For future information, the health food store is seen to be the preferred source for nonusers as well as for users. Nurse or midwife comes in second place in both groups but after that, users seem to rely on family and friends instead of other health care personnel, while nonusers prefer health care personnel. Discussion The use and the user of herbal remedies during pregnancy Herbal remedies were found to be used by 57.8% of the participants. This is quite a high percentage compared to most

790 Table 3. The Most Commonly Used Herbs in Pregnancy Among 578 Women at the Norfolk and Norwich University Hospital Antenatal Clinic Herb Ginger Cranberry Raspberry leaf Chamomile Floradix (iron-rich herbs) Echinacea Peppermint Lavender Fennel Nettle Number of users 157 144 137 76 44 25 21 11 8 7 % of the 334 users 47.0 43.1 41.0 22.8 13.2 7.5 6.3 3.3 2.4 2.1 % of all 578 participants 27.2 24.9 23.7 13.1 7.6 4.3 3.6 1.9 1.4 1.2

HOLST ET AL.

Most common indication Nausea=sickness Urinary tract infection (prevention or treatment) Prepare uterus=cervix for labor Relax=help sleep Iron supplement Prevent=treat cold Indigestion Help sleep Indigestion Detoxication

other studies of similar size. Australian studies performed in antenatal clinics found 12%12 and 36%,19 respectively. An American study from a rural obstetric clinic17 found 45.2% and another American study from a postnatal ward18 looked at complementary and alternative treatment in general and found 4.1% only. The Norwegian study (performed as interviews no more than 3 days after delivery), which this study was based on, found 36% users of herbal remedies.10 Ginger was used by almost half of the users in this study, which is high compared to other surveys and may be explained by the very common use of ginger in biscuits and beer in the United Kingdom. Cranberry was also used by a much higher percentage in this study than in any other: 43.1% versus 28.7%,17 8.3%,10 and 24.1%.19 Conversely, peppermint was used by only 6.3% of the users here compared to 39.8% in an American study17 and echinacea by 7.5% compared to 22.9% in Norway.10 A review of four studies on the effect of ginger against nausea and vomiting during pregnancy concludes that 1 g of ginger daily is more effective than placebo and that no adverse outcomes or side-effects were detected for the 3 weeks duration of the study.23 Interestingly, however, GraviFrisk (which translates to something like PregnaWell and equates to a daily dose of 6 g of dried ground ginger), which was advertised for pregnant women in Denmark, was withdrawn

from the market in February 2008 due to inadequate scientic documentation of its safety.24 The Danish Veterinary and Food Administration stated that it is not dangerous to consume food containing ginger, but that the amount in different herbal products is too high.24 The intention was to study various characteristics for the participants to be able to describe the most typical user of herbal remedies in pregnancy. The developed model showed that mothers with a university degree and being in their second or higher-order pregnancy were three times more likely to self-treat with herbal medicines. This nding is in line with other studies.9,18,19 Of perhaps greatest concern was the nding that 76% of the pregnant women reported not informing their doctor that they were utilizing herbal medicines, and reasons for this require elucidation. Frequencies of informing the doctor ranging from 33% to 52% are reported in other countries.25,26 Self-report should be improved to enable prescribers to ascertain the patients symptoms, seek advice on the safety of the herbal medicines on the patients behalf, and prevent any interactions with any prescribed medicine. In Sweden, a question regarding herbal remedies use is included in the standard questions all pregnant women are asked when attending their antenatal clinic. The information is then Table 5. Sources Preferred for Future Information About Herbs

Table 4. Sources of Information for Products Actually Used During Pregnancy Source 1) n 259 Family or friends My own idea Newspaper or magazine Health food store Doctor Alternative therapist Pharmacist Nurse or midwife Other Internet Books Number of women (%)a

Source 2) n 501

Number of women (%)a Nonusers n 194 72 (37.1) 35 (18.0) 115 104 54 87 104 27 22 (59.3) (53.6) (27.8) (44.8) (53.6) (13.9) (11.3) 0 Users n 307 150 (48.9) 81 (26.4) 186 107 92 105 151 66 48 15 (60.6) (34.9) (30.0) (34.2) (49.2) (21.5) (15.6) (4.9) All 222 (44.3) 116 (23.2) 301 211 146 192 255 93 70 15 (60.1) (42.1) (29.1) (38.3) (50.1) (18.6) (14.0) (3.0)

160 83 47 20 20 15 5 58 18 3 9

(61.8) (32.0) (18.1) (7.7) (7.7) (5.8) (1.9) (22.4) (6.9) (1.2) (3.5)

Family or friends Newspaper or magazine Health food store Doctor Alternative therapist Pharmacist Nurse or midwife Other Internet Books

a Please note that the percentages add up to more than 100 as more than one source could be given.

a Please note that the percentages add up to more than 100 as more than one source could be given.

USE OF HERBAL REMEDIES IN PREGNANCY collated and available from a database at the Swedish Medical Birth Register.27 Health-seeking behavior of users and nonusers of herbal remedies during pregnancy The most important source of information about herbal remedies was found to be family and friends, which is similar to other ndings8,10,19 and is of some concern as there is no reason to believe that these persons are competent to give advice on herbs to pregnant women. The sources of information that women would seek in the future differ from those they actually used in pregnancy. The reason for this discrepancy could be an easier access or a lower threshold to discuss use of herbal remedies with family and friends compared to health care personnel. The preferred future source was health food shops. This is similar to the nding in the Norwegian study.10 This is also of some concern as the competence of the personnel in health food shops is unclear. A small study performed by the Norwegian Consumer Council in 200228 concluding that only 2 of 12 employees in randomly selected health food shops in Norway could give correct answers to four basic questions regarding herbal remedies and an American study on customers to one separate herbal shop29 concluded that the employees had no particular training in pharmacology, physiology, or herbalism. No such research has been undertaken in the United Kingdom, although similar ndings would be expected as herbal remedy shops are unregulated and there is no requirement for staff training. Only one third of users reported that they had been advised by health care professionals to use herbal remedies. Research in other countries has found that Western-trained medical practitioners generally have little knowledge of herbal remedies, their safety, or potential interactions,30,31 and this may provide one reason for only one third recommending this course of action. The results do, however, require consideration with respect to the studys limitations. The results may not be generalizable with a 56% response rate, and women who were more interested in herbal drugs may have been more eager to ll out and return the questionnaire. Consequently, this could have overestimated the prevalence of herbal drug use. Conversely, the identied prevalence may be underestimated, with the survey being undertaken in the middle of pregnancy, and use later than the 20th week will not be identied. For ethical reasons, the researcher was only allowed to approach patients who had given verbal consent to the clinic receptionist, and therefore consent to participate was not sought from all attendees. Finally, the research was also only carried out in one hospital in one region in the United Kingdom; consequently, the respondents may not be representative of pregnant women in the United Kingdom. Conclusions More than half of women attending one antenatal clinic in the East of England reported using herbal remedies during pregnancy: mostly ginger, cranberry, raspberry leaves, and chamomile. Although the clinic provided care for patients from both deprived and afuent areas, the behavior may not

791 be generalizable for the rest of the United Kingdom. A nationwide survey is probably warranted to obtain a complete picture. Doctors or midwives were rarely informed about use of herbal remedies during pregnancy. One possible reason could be that health care personnel are not expected to be open to discuss such use or have adequate knowledge about herbal remedies. It would, however, seem appropriate for all health care professionals to be educated and aware of herbal remedy use during pregnancy. Certain patient groups are more likely to use herbal remedies during pregnancy; however, this should not prevent all patients from being questioned regarding herbal medicine use. With few exceptions, there is still a lack of well-conducted studies on the safety of herbs during pregnancy. As use of herbal remedies is so widespread during pregnancy, this should be a prioritized area of future research. Acknowledgments The authors want to thank everyone working in the antenatal clinic and antenatal ultrasound department at the Norfolk and Norwich University Hospital. A special thanks to the receptionists, without whom the study would not have been possible. Disclosure Statement No competing nancial interests exist. References
1. Nelson-Piercy C. Treatment of nausea and vomiting in pregnancy. When should it be treated and what can be safely taken? Drug Safety 1998;19:155164. 2. Santiago JR, Nolledo MS, Kinzler W, Santiago TV. Sleep and sleep disorders in pregnancy. Ann Intern Med 2001;134:396 408. 3. Richter JE. Gastroesophageal reux disease during pregnancy. Gastroenterol Clin North Am 2003;32:235261. 4. Jewell DJ, Young G. Interventions for treating constipation in pregnancy. Cochrane Database Syst Rev 2001;2:CD001142. 5. Stone P, Cook D, Hutton J, et al. Measurement of bloodpressure, edema and proteinuria in a pregnant population of New Zealand. Aust NZ J Obstet Gyn 1995;35:3237. 6. Milman N. Prepartum anaemia: Prevention and treatment. Ann Hematol 2008;87:949959. 7. Krcmery S, Hromec J, Demesova D. Treatment of lower urinary tract infection in pregnancy. Int J Antimicrob Ag 2001;17:279282. 8. Hollyer T, Boon H, Georgousis A, et al. The use of CAM by women suffering from nausea and vomiting during pregnancy. BMC Compl Alt Med 2002;2:5. 9. Hepner DL, Harnett M, Segal S, et al. Herbal medicine use in parturients. Anesth Analg 2002;94:690693. 10. Nordeng H, Havnen GC. Use of herbal drugs in pregnancy: A survey among 400 Norwegian women. Pharmacoepidemiol Drug Saf 2004;13:371380. 11. Koren G, Bologa M, Long D, et al. Perception of teratogenic risk by pregnant women exposed to drugs and chemicals during rst trimester. Am J Obstet Gynecol 1989;160:1190 1193. 12. Pinn G, Pallett L. Herbal medicine in pregnancy. Complement Ther Nurs Midwifery 2002;8:7780.

792
13. Tsui B, Dennehy CE, Tsourounis C. A survey of dietary supplement use during pregnancy at an academic medical centre. Am J Obstet Gynecol 2001;185:433437. 14. Westfall RE. Use of anti-emetic herbs in pregnancy: Womens choices, and the question of safety and efcacy. Complement Ther Nurs Midwifery 2004;10:3036. 15. Sweetman SC, ed. Martindale: The Complete Drug Reference 35th edition. London: Pharmaceutical Press, 2007. 16. Gibson P, Powrie R. Herbal and alternative medicine use during pregnancy: A cross-sectional survey. Obstet Gynecol 2001;97:44s45s. 17. Glover GD, Amonkar M, Rybeck BF, et al. Prescription, over-the-counter and herbal medicine use in a rural, obstetric population. Am J Obstet Gynecol 2003;188:10391045. 18. Refuerzo JS, Blackwell SC, Sokol RJ, et al. Use of overthe-counter medications and herbal remedies in pregnancy. Am J Perinat 2005;22:321324. 19. Forster D, Denning A, Wills G, et al. Herbal medicine use during pregnancy in a group of Australian women. BMC Pregnancy Childbirth 2006;6:21. 20. Byrne MJ, Semple SJ, Coulthard KP. Complementary medicine use during pregnancy. Interviews with 48 women in a hospital antenatal ward. Aust Pharmacist 2002;21:954959. 21. Maats FH, Crowther CA. Patterns of vitamin, mineral and herbal supplement use prior to and during pregnancy. Aust N Z J Obstet Gynecol 2002;42:494496. 22. Nordeng H, Havnen GC. Impact of socio-demographic factors, knowledge and attitude on the use of herbal products in pregnancy. Acta Obstet Gynecol Scand 2005;84:2633. 23. Bryer EA. Literature review of the effectiveness of ginger in alleviation mild-to-moderate nausea and vomiting of pregnancy. J Midwifery Wom Heal 2005;50:e1e3. 24. Danish Veterinary and Food Administration. The Danish Veterinary and Food Administration Warn Against Food Supplements Containing Ginger for Pregnant Women [in

HOLST ET AL.
Danish]. Online document at: www.foedevarestyrelsen.dk= Nyheder=Pressemeddelelser=2008=gravideogingefaer.htm Accessed November 17, 2008. Kennedy J. Herb and supplement use in the US adult population. Clin Ther 2005;27:18471858. Thomas K, Coleman P. Use of complementary or alternative medicine in a general population in Great Britain. Results from the National Omnibus survey. J Public Health 2004; 26:152157. Holst L, Nordeng H, Haavik S. Use of herbal drugs during early pregnancy in relation to maternal characteristics and pregnancy outcome. Pharmacoepidemiol Drug Saf 2008;17: 151159. Ebne HV. Dangerous advice in the health food shops [in Norwegian]. Forbruker-rapporten 2003;8:46. Archer EL, Boyle DK. Herb and supplement use among the retail population of an independent, urban herb store. J Holist Nurs 2008;26:2735. Suchard JR, Suchard MA, Steinfeldt JL. Physician knowledge of herbal toxicities and adverse herb-drug interactions. Eur J Emerg Med 2004;11:193197. Giveon SM, Liberman N, Klang S, et al. A survey of primary care physicians perceptions of their patients use of complementary medicine. Complement Ther Med 2003;11:254260.

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28. 29.

30.

31.

Address correspondence to: Lone Holst, M.Sc.Pharm Department of Chemistry=Centre for Pharmacy University of Bergen gaten 41 Alle N-5007 Bergen Norway E-mail: lone.holst@farm.uib.no