Kiwi

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Code: f84
Latin name: Actinidia deliciosa
Source material: Fresh fruit
Family: Actinidiaceae (Dilleniaceae)
Common names: Kiwi, Chinese gooseberry, Kiwifruit, Monkey peach, Sheep peach

Synonyms: A. latifolia var. deliciosa, A. chinensis deliciosa

There are 2 common species of Kiwi commercially available:

A. chinensis - Gold kiwi

A. deliciosa - Green kiwi (Chinese gooseberry)

Food

A food, which may result in allergy symptoms in sensitised individuals.

Allergen Exposure

The kiwi fruit (or kiwi) is the edible berry of a cultivar group of the woody vine A. deliciosa, and hybrids between this and other species in the genus Actinidia. (1) This interesting species is native to the Yangtze Valley, China. It was cultivated on a small scale at least 300 years ago, but most of the crop is derived from wild vines, even today. The Chinese have never shown much interest in exploiting the fruit. Kiwi was developed commercially in New Zealand and named after the national bird. Commercial crops are grown mainly in New Zealand, the United States and France. However, kiwi fruit is a latecomer to Western cuisines, and the extent of its use varies radically according to fashion.

The Kiwi plant is a tough, woody, deciduous twining vine or climbing shrub. The oblong fruit, up to 8 cm long, has russet-brown skin densely covered with short, stiff brown hairs. The flesh is usually bright green and pleasantly acidic in flavour. The minute, dark-purple or nearly black seeds are unnoticeable in eating. (1)

Gold kiwis have a smooth, bronze skin, a pointed cap at one end, and distinctive golden-yellow flesh, with a less tart and more tropical flavour than that of green kiwi. Gold kiwi is less hairy than the green cultivars, and can be eaten whole after rubbing off the thin, fluffy coat. Green kiwi skin is thick and unpalatable.

Kiwis are available year-round, due to storage. The fruits are eaten fresh or may be added to meat dishes, pies, puddings or cakes. As Kiwi contains enzymes similar to Papain, the raw fruit can act as a meat tenderiser. After peeling (usually with lye), fruits are canned, frozen, or freeze-dried. Kiwi is used in sauces, jams, ice creams, breads and various beverages, including wine. Blending with apple juice or malic acid tends to be important in kiwi processing, for reduction of kiwis’ acidity. Slightly underripe fruits, which are high in pectin, are chosen for making jelly, jam and chutney. (1)

The Chinese regard the kiwi as a tonic for growing children, and for women after childbirth. (1)

Because of shortages of the bees needed for pollination, pollen may be sprayed onto the plants in a suspension.

Allergen Description

An evaluation of the allergenicity of 6 different kiwifruit cultivars using prick-to-prick testing, open food challenges, and ELISA, reported that some varieties may be less allergenic than the common green kiwifruit, and that patients with kiwifruit allergy may be able to tolerate these varieties. (2)

At least 12 allergenic proteins have been detected in Kiwi fruit, ranging from 12 to 64 kDa in size. The allergens of 12, 24, 28 and 30 kDa appeared to be the most important. Only the 30 kDa protein was recognised by sera of 100% of patients, and was later characterised as the major protein Act c 1, a protein which also exists in the closely-related family member A. deliciosa. (3, 4, 5) A 43 kDa protein, only partially characterised, has been isolated and shown to account for only 0.1% of total kiwi protein content. (6) In a study of 76 patients with a history of kiwi allergy, of whom 23 had had a positive DBPCFC, serum IgE bound to 12 protein bands in kiwi protein extract. A protein band with a molecular weight of 38 kDa was the major allergen, recognised by 59% of the patients. Unlike in other studies, which had reported actinidin (Act d 1) as a major allergen, IgE did not bind to actinidin in this extract, or to purified native or recombinant forms of actinidin. The study concluded that major allergens in a patient group may not necessarily be recognised in another. (7)

The protein content of kiwi increases during the ripening process. Importantly, different protein patterns have been demonstrated in green and in gold kiwi. In green kiwi, actinidin and kiwellin were the major components. Thaumatin-like protein was found in high amounts in both green and gold kiwi. Variations in the relative amounts of the proteins, as well as new protein bands, were seen during the ripening process of green kiwi and, to a lesser extent, of gold kiwi. Similarly, after ethylene exposure (with or without previous cold storage), the relative amount of some protein bands varied, especially in green kiwi. (8) Other studies have demonstrated similar results. (9, 10) Despite having different protein profiles and IgE-binding patterns, the 2 species have proteins that extensively cross-inhibit the binding to IgE. (10) However, the relevance of these differences may be complex. In 90 Kiwi-allergic individuals, IgE studies showed marked differences in the allergen compositions of green and gold kiwi extracts. Phytocystatin (Act d 4) and a thaumatin-like protein (Act d 2) were identified as allergens common to both cultivars. Two allergens with homology to chitinases were found in gold kiwi, whereas actinidin (Act d 1) was detected exclusively in green kiwi. Patients from Central Europe and central Italy showed distinct sensitisation profiles towards green and gold kiwi, as well as actinidin; and whereas sera from Austrian and Dutch patients mainly recognised green kiwi and actinidin, almost all Italian sera showed IgE binding to both kiwi species, but only half of them contained actinidin-specific IgE. Green and gold kiwi extracts were shown to be highly cross-reactive in inhibition studies. This implies that gold kiwi may be tolerated by patients exclusively sensitised to Act c 1. (9)

The following allergens have been characterised:

Act d 1, a 30 kDa protein, also known as actinidin, belonging to the cysteine protease protein family. (4, 7, 9, 11, 12, 13, 14, 15, 16, 17, 18, 19, 20)

Act d 2, a 24 kDa thaumatin-like protein. (9, 11, 12, 13, 14, 15, 16, 19, 20, 21, 22, 23)

Act d 3, a 40 kDa protein. (11, 14)

Act d 4, a 11 kDa protein, a phytocystatin, a cysteine protease inhibitor. (9, 11, 24, 25, 26)

Act d 5, also known as kiwellin, a 26-28 kDa protein. (11, 4, 24, 27, 28, 29)

Act d 6, a pectin methylesterase inhibitor. (11, 30, 31, 32, 33)

Act d 7, a 50 kDa protein, a pectin methylesterase. (11, 30, 32)

Act d 8, a Bet v 1 homologue. (11)

Act d 9, a profilin. (5, 11, 34)

Act d 10, a lipid transfer protein. (11, 35, 36)

Act d 11, a Bet v 1-like homologue. (11, 37)

A class 1 chitinase (38) and a glycosyl hydrolase have been isolated. (39)

Actinidin has physical and chemical properties similar to those of Papain, which may perhaps explain some hypersensitivity reactions. (40)

Act c 2 (from A. chinensis), the thaumatin-like defence protein, was shown to be a rapidly digestible protein, eliciting positive skin-specific IgE responses in 4 (80%) of 5 patients with oral allergy syndrome. (12)

Act c 5, from A. chinensis, accounts for approximately a third of gold kiwi total protein content. (41)

Studies have reported that patients with systemic reactions showed IgE binding to digestion-resistant allergens, but that patients with oral symptoms reacted only to digestion-labile allergens. Furthermore, an increase in pH from 1.5 to 2.5 significantly reduced pepsin breakdown of kiwi allergens, and the study suggested that patients with hypoacidic gastric conditions are at increased risk of systemic absorption of allergens. (42) Moreover, Act d 1 and Act d 2 appear to display nearly unchanged IgE binding abilities following simulated gastric digestion. (13) Although heat may deactivate many kiwi allergens, heat-stable allergens may still result in adverse reactions being elicited. (20)

A heterogenous response to the various Kiwi allergens can be expected. This is illustrated by a number of studies. For example, in a study examining purified Act d 28kD (Act d 5), Act d 1 and Act d 2, with 30 sera of 30 kiwi-allergic patients, 10 (33%) patients showed IgE reactivity to Act d 28kD, 14 (47%) to Act d 1, and 9 (30%) to Act d 2. Different profiles of IgE binding were observed. Combined reactivity to the 3 kiwi allergens was shown in 2 subjects (6.6%). Four subjects (13.3%) recognised Act d 1 and Act d 2, whereas 4 and 3 subjects (13.3% and 10%) showed reactivity to Act d 1 plus Act d 28kD, and Act d 2 plus Act d 28kD, respectively. Sera of 5 (Act d 1, 16.6%), 4 (Act d 28kD, 13.3%), and 2 (Act d 2, 6.6%) subjects recognised a single allergen. Importantly, 8 (26.6%) subjects were negative to all 3 kiwi proteins. (16)

Similarly, in a study of 43 patients with allergy symptoms who were sensitised to kiwi, of whom 33 were evaluated with DBPCFCs (and of whom 23 were positive), the most frequent clinical manifestation was oral allergy syndrome. Twenty-one per cent of the patients were not allergic to pollen. Forty-six per cent of the patients experienced systemic symptoms, which occurred with higher frequency in patients not allergic to pollen (100%). Twenty-eight per cent of the patients were sensitised to latex. The IgE-binding bands in kiwi extract more frequently recognised by patient sera were those of 30, 24, 66, and 12 kDa. No allergens could be associated with any particular pattern of Kiwi-induced allergic reactions, confirming that Kiwi allergy is not a homogeneous disorder, but consists of several clinical subgroups. (19)

Ninety patients with kiwi allergy from Austria, central Italy, and the Netherlands, most of them having OAS and associated systemic symptoms, were tested for IgE binding to green and gold kiwi protein extracts and to purified actinidin. Differences between allergens recognised by sera from northern European countries and sera from Italian patients were demonstrated. Actinidin (Act c 1) was recognised by IgE from almost all the Northern European patients, but by less than 50% from Italian patients. (9)

In a study that aimed to isolate major kiwi allergens utilising sera of 92 kiwi-sensitised Spanish patients with different clinical symptoms, 3 major IgE-binding proteins were isolated and identified as actinidin Act d 1, the thaumatin-like Act d 2 and Act d 3.02. Specific IgE to each of the 3 allergens was found in over 60% of sera from kiwi-sensitised patients, and Act d 1 and Act d 2 induced positive SPT responses in over 50% of the tested patients. A significant link was uncovered between IgE levels to Act d 1 and Act d 3, and anaphylaxis: severe symptoms after kiwi ingestion were associated with high IgE levels to Act d 1 and Act d 3. (14)

A German study of 25 subjects with birch pollen and kiwi allergy reported that 23 had localised oral symptoms and 2 had urticaria. Sensitisation was demonstrated to a 67 kDa allergen in 55%, a 43 kDa in 68%, a 30 kDa in 19%, a 22 kDa in 31%, and a 13 kDa in 9%. (43)

Of 12 latex-allergic patients with kiwi allergy, 9 were sensitised to kiwellin (Act d 5), and 4 to cystatin (Act d 4). Of 38 sera from patients with multiple pollen and Kiwi allergy, 25 (68%) were shown to have IgE specific to kiwellin and 23 (54%) to cystatin. (24)

Potential Cross-Reactivity

Extensive cross-reactivity between the different individual species of the genus could be expected; but manifestations are variable, depending on allergen composition, as described above. (44)

The association of kiwi allergy with allergies to pollen and latex has been described, and cross-reactivity has been confirmed by inhibition studies with birch pollen, (3, 43, 56, 60, 45) Timothy pollen, (3) avocado, (38, 46) banana, (46, 47) latex, (38, 46) rye, (48) and hazelnut. (48) Kiwi allergy has also been associated with grass allergy, as in a Northern Italian study that reported grass pollen to be the most common pollen allergy, and to be frequently associated with oral allergic syndrome (OAS). In 56 children with respiratory allergy due to grass pollen, 5 of the 14 cases (36%) sensitised to Bet v 1 showed food allergy, and 8 (57%) food sensitisation; 6 (46%) of the 13 children sensitised to Bet v 2 showed food allergy, and 7 (54%) food sensitisation. Among the 16 patients with food allergy, hazelnut was the major triggering food (50%), followed by peanut (38%), kiwi (31%), apple and walnut (19%). (49) Oral allergy syndrome to kiwi associated with Japanese cedar pollen allergy has been reported. (50)

Specific Kiwi allergens may play a role in cross-reactivity between kiwi, other foods, and pollens.

The kiwi allergen Act c 1 appears to cross-react with thiol proteinases, e.g. bromelain and Papain, from papaya and pineapple. (40, 51) In a study of 20 patients with occupational asthma (baker's asthma) caused by wheat flour inhalation, ingestion of kiwi elicited oral allergy syndrome in 7 (35%). Skin- and serum-specific IgE for kiwi was found in all of these kiwi-allergic patients, and IgE to Act d 1 and Act d 2 was detected in 57% and 43%, respectively. The authors suggested that cross-reactive carbohydrate determinants and thiol-proteases (bromelain) homologous to Act d 1 were responsible for wheat-kiwi cross-reactivity in some patients. (15)

Cross-reactivity between the thaumatin-like protein Act c 2 and other fruits or vegetables containing this protein could be expected. (52)

Cross-reactivity between kiwi and plants containing profilin (5, 34, 53) or lipid transfer protein (35, 54) can also be expected. Timothy, rye, mugwort (Artemisia vulgaris) and birch pollen have been reported to show strong cross-reactivity with some kiwi allergens, suggesting complete identity between certain food and pollen allergens. (55, 56, 57) Cross-reactivity demonstrated between birch pollen and kiwi allergens was due to a 10-12 kDa protein, which would appear to be a profilin. (3, 5, 56) Studies have reported a high prevalence of kiwi allergenicity in birch-allergic individuals, but other studies have not concurred. In a Japanese study of 171 birch pollen-sensitised individuals (CAP positive > or = 2), 6 (3.5%) were shown to be hypersensitive to kiwi fruit. In a study of 253 patients with birch pollen sensitisation, as measured by specific IgE, 3 (1%) were shown to be hypersensitive to kiwi fruit. (58) Some authors have suggested that cross-reactivity between kiwi and birch pollen is due mainly to carbohydrate moieties that are said to have a much weaker cross-reactivity. (59) Interestingly, patients with birch pollen allergy and without clinical signs of kiwi allergy may show positive skin-specific IgE to kiwi, and patients with kiwi allergy have higher specific IgE to birch pollen, compared to patients with isolated birch pollen allergy. (60)

Approximately 30-50% of individuals who are allergic to natural rubber latex (NRL) show an associated hypersensitivity to some plant-derived foods, especially fresh fruits. This association of latex allergy and allergy to plant-derived foods is called latex-fruit syndrome. (38, 61, 62, 63, 64, 65, 66, 67) An increasing number of plant sources, such as avocado, banana, chestnut, kiwi, peach, tomato, potato, bell pepper and custard apple, have been associated with this syndrome. (68, 69, 70) Kiwi and NRL cross-reactivity is common, with 17% of latex-allergic individuals being sensitised to this food. (71, 72) Approximately 12.2% of NRL-allergic individuals appear to be kiwi-allergic. (73) Several types of proteins have been identified as being involved in latex-fruit syndrome. (46) A plant-defence protein – a class I chitinase (which cross-reacts with hevein [Hev b 6.02]) and a major IgE-binding allergen for patients allergic to NRL – is probably the most important allergen responsible for cross-reactions between kiwi and latex; (74) but other panallergen-like proteins, e.g. patatin, may also play a role, (72) – including Hev b 5, a NRL protein probably responsible for anaphylaxis in NRL-allergic individuals; this allergen has significant homology with kiwi and potato. (75, 76) Other allergens may also play a role: Ole e 10 – a glycosyl hydrolase, and a major allergen in olive pollen – has a 53% identity with Ole e 9, a 1,3-beta-glucanase. Ole e 10 shares IgE B cell epitopes with proteins from a number of pollens, including latex, tomato, kiwi, potato, and peach, and may therefore be a candidate for involvement in pollen-latex-fruit syndrome. (39)

Cross-reactivity between the latex from leaves of Ficus benjamina (weeping fig), fig and (to a lesser extent) Kiwi has been reported. (77) In a study of 54 Ficus benjamina-sensitised individuals, sensitisation was specifically associated with positive skin tests to fresh fig (83%), dried fig (37%), kiwi (28%), papaya (22%), avocado (19%), banana (15%), and pineapple (10%). This cross-reactivity is mediated at least in part by thiolproteases, ficin and Papain. (78)

From a study reporting reduced IgE binding to kiwi and celery in RAST inhibition studies, the presence of a 60 kDa allergen distinct from Bet v 1 and profilin has been deduced. It was suggested that this was a novel cross-reactive allergen that may also contribute to symptoms of oral allergy syndrome. (79)

Other cross-reactive associations between kiwi and other plants have been reported. Of 134 patients with allergy to olive pollen, 40 reported adverse reactions to plant-derived food. Skin-specific IgE and oral challenges confirmed allergy to a number of foods, including kiwi. The cross-reactive allergen may be associated with the olive pollen allergen Ole e 3. (80) Kiwi allergy has also been reported to be commonly associated with allergy to melon. (81) Allergy to kiwi, poppy seed, and/or sesame seed has also been reported to occur often in patients with a simultaneous sensitisation to nuts and flour. These cross-reactions were verified by RAST inhibition studies. Further studies demonstrated that the degree of cross-reactivity between kiwi, sesame, poppy seed, hazelnut, and rye grain was found to be very high in the patients studied. The existence of both cross-reacting and unique components was observed; however, the cross-reacting and unique components could be different for different patients. (48)

Cross-reactivity between an isolated 24 kDa kiwi allergen and Fes p 4 (Fescue meadow pollen) was confirmed by anti-grass group 4 moab 2D8. (82)

Clinical Experience

IgE-mediated reactions

Acute allergy to kiwi fruit was first described in 1981: a 53-year-old atopic woman developed urticaria, wheeze and laryngeal oedema on handling kiwi. (83) Since then, there have been reports of kiwi allergy presenting with a wide range of symptoms, from localised oral allergy syndrome (OAS) to life-threatening anaphylaxis. (40, 58, 59, 84, 85, 86, 87, 88, 89, 90, 91, 92) As kiwi is a new food in many countries, and dietary habits vary from one locale to another, the prevalence of allergy to kiwi may be much more common in some countries than in others.

A questionnaire-based survey conducted in Toulouse schools in France found that, out of 2 716 questionnaires returned, 192 reported a food allergy, and that kiwi was the third-most-often-reported, purportedly causing allergic symptoms in 22 (9.0%) cases. (93)

A study was conducted at 17 clinics in 15 European cities to evaluate the differences between some northern countries regarding what foods, according to food-allergic patients, elicit hypersensitivity symptoms. It was reported, after evaluation of questionnaires concerning 86 different foods, that the foods apparently most often eliciting symptoms in Russia, Estonia, and Lithuania were citrus fruits, chocolate, honey, apple, hazelnut, srawberry, fish, tomato, hen’s egg, and milk; these results differed from those of Sweden and Denmark, where birch pollen-related foods – such as nuts, apple, pear, kiwi, stone fruits, and carrot – were the most common reported causes. The most common symptoms reported were oral allergy syndrome and urticaria. Birch pollen-related foods apparently dominated as allergens in Scandinavia, whereas some mugwort-related foods seemed to be of more importance in Russia and the Baltic States. Among 1 139 individuals, kiwi was the fifth-most-commonly reported food allergen, resulting in adverse effects in 32%. (94)

The most common symptoms attributed to kiwi allergy are those associated with oral allergy syndrome, which include pruritis of the eyes, ears, tongue, pharynx and mouth, and swelling of the lips, tongue and pharynx. (12, 50, 58, 95) Symptoms of oral allergy syndrome from kiwi fruit once resulted from a lover's kiss. (96) Many other allergic symptoms are also possible: nausea, vomiting, diarrhoea, abdominal pain, asthma, angioedema, allergic contact dermatitis, atopic dermatitis and contact urticaria have also been reported. (97, 98, 99) Sensitisation to kiwi skin has been documented. (100) Allergy to kiwi is often associated with latex allergy, as described in the Potential Cross-Reactivity section above.

Although OAS has been reported to occur with kiwi, a Japanese study of sensitisation to Japanese cedar, orchard grass, short ragweed, and alder tree pollen among 1 067 paediatric patients with allergic diseases – among whom 16 cases of childhood OAS were identified and further explored – the most frequent allergen resulting in OAS was kiwi, followed by tomato, orange and melon. The study found that childhood OAS was not associated with pollen allergy, as was seen with adults. (101)

No specific allergens could be associated with any particular pattern of kiwi-induced allergic reactions, confirming that kiwi allergy is not a homogeneous disorder, but consists of several clinical subgroups. (19) Studies and case reports are illustrative.

In a British study of 273 subjects with a history suggestive of allergy to kiwi, the most frequently reported symptoms were localised to the oral mucosa (65%); but severe symptoms (wheeze, cyanosis or collapse) were reported by 18% of subjects. Young children were significantly more likely than adults to react on their first known exposure, and to report severe symptoms. Twenty-four of 45 subjects (53%) evaluated by DBPCFC had allergy confirmed. A prick-to-prick skin test with fresh kiwi was positive in 93% of subjects who had allergy confirmed by DBPCFC, and also in 55% of subjects with a negative food challenge. The commercial extract was significantly less sensitive, but with fewer false-positive reactions. Serum-specific IgE was positive in only 54% of subjects who had a positive challenge. (90)

A 26-year-old patient with a localised pruritic reaction a few minutes after eating kiwi fruit has been described; a similar incident happened a few months later, accompanied by dysphagia, vomiting and urticaria. (102)

A German study of 25 subjects with birch pollen and kiwi allergy reported that 23 had localised oral symptoms and 2 had urticaria. (43)

In a prospective trial of 20 children with a history of immediate allergic reactions to kiwi, who underwent double-blind, placebo-controlled food challenges with fresh, steam-cooked and industrially homogenised kiwi, fresh kiwi induced positive skin-prick wheals in all the children. Sera from all children showed specific IgE to raw kiwi, and 1 to the homogenised preparation. Act c 1 and Act c 2 were the major allergens identified. Clinical reactivity following challenge with heated kiwi was negative, except for 1 child who developed symptoms. (20)

Numerous instances of anaphylaxis to kiwi fruit have been reported, (103, 104, 105, 106, 107, 108) including in a 12-year-old boy who initially experienced localised oral symptoms, vomiting, urticaria and dizziness. (109) A 57-year-old man, who had experienced 2 anaphylactic reactions when eating kiwi, had a severe systemic reaction on skin-testing performed at home by his daughter. (110) A 29-year-old woman described several episodes of severe anaphylaxis after consumption of kiwi fruit, including 3 episodes of allergic shock with loss of consciousness and subsequent hospitalisation. During the first 2 episodes, the symptoms started shortly after ingestion of fresh kiwi alone, and the third episode was elicited by minute amounts of kiwi left on a knife that was subsequently used to prepare a strawberry dessert served to the patient in a restaurant. (106)

Food-dependent exercise-induced anaphylaxis to kiwi has also been reported. (111)

Of 22 patients allergic to kiwi fruit, 10 with severe systemic reactions and 12 with localised symptoms confined to the oral and pharyngeal mucosa (oral allergy syndrome), skin-specific IgE was positive to kiwi fruit in all, whereas serum-specific IgE to kiwi was present only in those with generalised severe symptoms. Surprisingly, all 22 patients with clinical kiwi allergy had skin-specific IgE and elevated serum IgE to birch pollen. Clinically, all complained of rhinitis during birch-pollen season. Many patients showed sensitisation to grass and mugwort pollen. Allergy to other foods was also found to be associated with kiwi allergy: strongly to apple and hazelnut, moderately to carrot, potato, and avocado, and weakly to wheat and rye flour, pineapple and papaya, and their enzymes bromelain and Papain. (60)

An association between allergy to kiwi and asthma has also been reported. Among 163 asthmatic children with food allergy and food-induced asthma, kiwi fruit was reported to have resulted in asthma in 3.6% following DBPCFC oral challenges to kiwi. (112)

Considering that adverse reactions to kiwi may be severe, the possibility that kiwi is a ‘hidden’ allergen needs to be considered in ‘idiopathic’ anaphylaxis. (113) Inadvertent contact with kiwi via kissing may need to be considered. (114)

Allergy to kiwi is reported to have resulted in acute pancreatitis in a 48-year-old man. (115)

Sensitivity of the measurements of serum IgE in kiwi-allergic patients was reportedly between 13% and over 70%, a range that may reflect the different kiwi-allergic populations being studied, and also the different techniques used to measure specific IgE. (43, 91)

Compiled by Dr Harris Steinman, harris@allergyadvisor.comin)

References

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Novembre E, Bernardini R, Bertini G, Massai G, Vierucci A. Skin-prick-test-induced anaphylaxis. Allergy 1995;50(6):511-3.

 

As in all diagnostic testing, the diagnosis is made by the physican based on both test results and the patient history.