Indonesian Journal of Life Sciences Vol. 02 | Number 01 | March (2020) http://journal.i3l.ac.id/ojs/index.php/IJLS/

REVIEW ARTICLE

Botanical Aspects, Phytochemicals and Health Benefits of Andaliman (Zanthoxylum acanthopodium)

Alfredo Oktavianto Natasutedja 1, Erika Lumbantobing 1, Emita Josephine 1, Lioni Carol 1, Decky Indrawan Junaedi 2, Suluh Normasiwi 2, Agus Budiawan Naro Putra 1*

1Department of Science and Nutrition, International Institute for Life Sciences, , Indonesia 2Cibodas Botanical Garden - Research Centre for Plant Conservation and Botanical Garden - LIPI, Cianjur, Indonesia

*corresponding author. Email: [email protected]

ABSTRACT

Andaliman (Zanthoxylum acanthopodium) is a specialty widely found in the Provinces of North and Aceh, Indonesia. The fruit is usually used by people in as a food ingredient to cook Batak’s such as , tombur, and naniura. It is also used as one of the ingredients to make Indonesian spicy called . Andaliman fruit is reported to eliminate the undesirable smell in fish and raw meat. Moreover, it could also reduce total volatile base nitrogen content in fish which helps to prevent spoilage. Furthermore, andaliman has been reported to contain bioactive compounds which act as antioxidant, antimicrobial, anti-inflammatory, anti-aging, anti-acne, and anti-halitosis effects. This review focuses on the botanical aspects of and health potential exhibited by andaliman.

Keywords: andaliman; bioactive compounds; health benefits; Zanthoxylum acanthopodium

INTRODUCTION has a comparably expensive price in local markets (Sibarani et al., 2013). Z. Andaliman (Zanthoxylum acanthopodium) acanthopodium is relatively complex to grow in is a specialty spice in Indonesia, which is cultivation, and many local farmers rely on commonly found in the Provinces of North naturally-grown seedlings from recommended Sumatra and Aceh. The species itself is burning lands rather than sowing its seeds by distributed particularly in Tapanuli, North themselves. Many natural populations occur in Sumatra, at 1500 m above sea level at high slope habitat (Siregar, 2010). The plant also temperature between 15 - 18°C (Muzafri et al., naturally occurs in rainforests and thickets at 2018). The fruit is usually used by Batak people low and mid-altitude (Hartley, 1966). The genus in North Sumatra as food ingredient, and it is an (Zanthoxylum) belongs to the Rutaceae family, economically important commodity because it and plants included in this genus are mainly

8

Indonesian Journal of Life Sciences Vol. 02 | Number 01 | March (2020) http://journal.i3l.ac.id/ojs/index.php/IJLS/

used as and medicinal agents (Wijaya et distinguished from the other genus in Rutaceae al., 2018). The genus has over 546 species from family for the combination of three characters: all over the world. Zanthoxylum piperitum armed, leaves alternate and compound (Japan), Zanthoxylum schinifolium (Korea), (generally pinnate), and carpels entirely or Zanthoxylum simulans (Taiwan), and partially distinct (Hartley 1966). Among the Zanthoxylum rhetsa (India) have been used as other Malesian Zanthoxylum species, Z. traditional spices due to the natural flavors that acanthopodium is clearly distinguished by their produce unique sensations in the mouth flattened and pseudostipular prickles. This (Wijaya et al., 2018); but not limited to the species is different from Zanthoxylum armatum utilization of the plants as medicinal agents. due to the observable leaflet main vein, the Z. acanthopodium could also prolonged color of the anthers prior to anthesis, and the shelf life of the fish-based , such as arsik, inflorescence that positioned in the axil of tombur, and naniura, due to its antioxidant and lateral leaves (Hartley 1966). antimicrobial activities. Andaliman could eliminate the undesirable smell in fish and raw Morphology and Structure meat (Muzafri et al., 2018), also reducing total There are three varieties of andaliman that volatile base nitrogen (TVBN) content. can be found in North Sumatra province, which Therefore preventing the spoilage of the fish. are renowned as sihorbo, simanuk, and sitanga. Andaliman produces strong tingling sensation These three varieties are commonly found in and citrus-like aroma (Wijaya et al., 2018). districts of Tapanuli, Tobasa, and Dairi. In Besides, andaliman is usually used as one of the specific, sihorbo has larger fruit, is less ingredients to make a chili-based paste which is aromatic, and is not produced in abundant known as sambal in Indonesia. amounts. Simanuk has smaller fruit, a sharper Andaliman has been reported to have aroma and taste, and a larger production yield. several health effects. Studies showed that Sitanga has a very strong fruit flavor yet less andaliman contains bioactive compounds which preferred due to its bug aroma (Napitupulu et act as antioxidant and radical scavenging al., 2004). activity, antimicrobial, anti-inflammatory, Z. acanthopodium plant is in the form of antipyretics, anti-halitosis, anti-aging and anti- shrubs or small trees that can grow up to 5 m. acne, and many else (Situmorang et al., 2019; This species has many spines on its stems and Muzafri et al., 2018; Hanum & Laila, 2016; compound leaves spread out 5-20 cm long and Suryanto et al., 2005). 3-15 cm wide. The upper surface color of the leaves is shiny green while the lower surface is BOTANICAL ASPECTS OF ANDALIMAN light green. The flowers are located on the Origin and Botanical Classification axillary buds and the plant itself is androgynous Andaliman (Zanthoxylum acanthopodium) which has staminate (pollen-producing male is naturally distributed in North India, Nepal, part) and carpellate (ovule-producing female Sikkim, East Pakistan, Burma, Thailand, and part) with a pale yellow color. The shape of the Southwest China. In Indonesia, this species only fruit is like pepper, small round, could be light occurs in Aceh and North Sumatra. Andaliman colored green and/or dark red (Siregar, 2003). It belongs to the genus Zanthoxylum, which could turn into black when it is dried (Muzafri et

9

Indonesian Journal of Life Sciences Vol. 02 | Number 01 | March (2020) http://journal.i3l.ac.id/ojs/index.php/IJLS/

al., 2018). The size of the fruit is 2-3 mm in BIOACTIVE COMPOUNDS AND EXTRACTION diameter with one seed in each fruit colored in TECHNIQUES shiny black and covered with hard skin (Siregar, According to Muzafri, Julianti & Rusmarilin 2003). Black andaliman usually has no typical (2018), andaliman fruit extract produced the flavor of andaliman compared to the green or highest yield when it is extracted with red andaliman. Red andaliman is the indication methanol, then followed by with ethyl acetate, that the andaliman fruit is ripened and as the water, and hexane (4.15%, 3.97%, 3.23%, and process goes on, it will turn into black (Wijaya 3.02%, respectively). These solvents worked for et al., 2018). different phytochemicals. Alkaloids can be extracted with methanol, ethyl acetate, and Cultivation hexane. Flavonoids, glycoside, and tannins can Andaliman was found growing wild and it be extracted with water, methanol, and ethyl has not been widely cultivated. Plants grow acetate. Saponins can be extracted with naturally from seeds dispersed by birds (Siregar, methanol, and ethyl acetate. 2010). Seeds can also be found near the old Triterpens/steroids can be extracted with trees in prescribed burns area, and in soil seed methanol and hexane, while glycoside bank of andaliman habitat (Nurlaeni and anthraquinone can only be extracted with Junaedi, 2018). Andaliman is known to be methanol (Muzafri, Julianti & Rusmarilin, 2018). difficult to propagate and shows a low The solvent used for extraction of bioactive germination rate. Furthermore, information compounds in andaliman determines the about andaliman cultivation technique is still stability of the compounds according to limited. An effort of andaliman propagation has Suryanto, E., Sastrohamidjojo, H., & Raharjo, S. been carried out in several studies. First, is the (2004). In addition, acetone and ethanol generative propagation, which requires extracts are heat- and light-stable. dormancy-breaking treatments including the use of warm water and the potassium nitrate HEALTH BENEFITS OF ANDALIMAN (KNO3) solution to soak the seeds (Siregar, Andaliman has been reported to exert 2010; Siregar, 2013). Secondly, is the vegetative health-beneficial effects. Researches showed propagation, which is using stem cutting of that andaliman contains several functional andaliman with additional plastic cover and properties including but not limited to plant growth regulators (Siregar, 2010). On the antioxidant activity, antimicrobial activity, anti- other hands, another vegetative technique has inflammatory, anti-aging and anti-acne, and been done which is known as in vitro culture. anti-halitosis effects. Purohit et al. (2019) reported that another Zanthoxhylum species (Z. armatum) could be Antioxidant Activity cultured by indirect organogenesis using aseptic Andaliman showed antioxidant activity leaf explants in liquid Woody Plant Medium when it is extracted with hexane, ethanol, and with various concentration of Thidiazuron. acetone. All extracts had 1,1-diphenyl-2-

picrylhydrazyl (DPPH) scavenging activity, with the highest anti-radical activity was shown by

10

Indonesian Journal of Life Sciences Vol. 02 | Number 01 | March (2020) http://journal.i3l.ac.id/ojs/index.php/IJLS/

ethanol-extracted andaliman. The antioxidant E. coli, Salmonella typhi, Staphylococcus aureus properties of andaliman is due to the presence and B. subtilis. Meanwhile, triterpenoids of flavonoid compound (Suryanto & Rahardjo, inhibited B. subtilis, S. aureus and E. coli. The 2004). Another study was done by evaluating examples of compounds in triterpenoids group the petroleum ether-extracted andaliman. are linalool, indole, and kadinen (Muzafri, However, the extract showed a weak Julianti & Rusmarilin, 2018). antioxidant activity compared to butylated hydroxytoluene (BHT) and quercetin that acted as the standards (Elenora Kristanty & Suriawati, 2014). A study conducted in 2015 generated results that andaliman extract had a lower antioxidant activity compared to that of Japanese pepper (Karnady, 2015).

Antimicrobial Activity

Extract of andaliman has been reported to Figure 1. Inhibition Zone of Ethyl Acetate Extract of contain alkaloids, flavonoids, glycoside, Andaliman in Different Concentration against Several saponins, tannins, triterpenoid/steroids, and Pathogenic Bacteria glycoside anthraquinones. The substances that Methanol-extracted andaliman had the provide the antimicrobial activity are highest yield (4.15%) followed by extraction flavonoids, alkaloids, and tannins. Phenolic with ethyl acetate (3.97%), water (3.23%), and compounds seem to have better antimicrobial hexane (3.02%). Moreover, water- and activities compared to flavonoids. Andaliman methanol-extracted andaliman gave the highest extract can be used to inhibit the growth of growth inhibition towards S. aureus and as the Escherichia coli, Staphylococcus aureus, concentration was getting higher, the inhibition Staphylococcus typhimurium (Guleria et al., zone increased. Ethyl acetate-extracted 2013), Bacillus stearothermophilus, andaliman was reported to give the best Pseudomonas aeruginosa and Vibrio cholera antimicrobial effect compared to other solvent (Muzafri, Julianti & Rusmarilin, 2018). (Sitanggang, Duniaji & Pratiwi, 2019; Wijaya, Phenolic and flavonoids also reported to Napitupulu, Karnady & Indariani, 2018). As have antifungal activity which can inhibit the shown in Figure 1, andaliman ethyl acetate growth of A. alternata and C. lunata (Guleria et extract showed inhibition effect to the growth al., 2013). Alkaloids are reported for its of S. typhimurium and gave highest antimicrobial activity against Staphylococcus antimicrobial activities with minimum inhibitory aureus, Streptococcus sanguis, Escherichia coli concentration (MIC) value of 0.5% as reported and Pseudomonas aeruginosa. Berberine, beta- by Muzafri et al. (2018). hydrastine, canadine and canadaline are Bacterial cell wall and porin protein of the compounds that are included in alkaloids group bacteria would affect their susceptibilities and were reported to have antimicrobial towards the compounds and solvents used activities (Muzafri, Julianti & Rusmarilin, 2018). which makes the result varies (Muzafri, Julianti As for the steroids, it prevented the growth of

11

Indonesian Journal of Life Sciences Vol. 02 | Number 01 | March (2020) http://journal.i3l.ac.id/ojs/index.php/IJLS/

& Rusmarilin, 2018). Andaliman extract can 2012). Exposure towards sunlight damages cause cell lysis by destroying the cell wall and collagen and leads to cell death. causing the intracellular metabolites to leak out Hanum & Laila (2016) reported that peel- by increasing the permeability (Parhusip, Jenie, off gel mask (PGM) of andaliman can help to Rahayu & Yasni, 2010). The permeability reduce skin pore size and remove dirt and dead increases due to the presence of phenolic cells from the skin. Formation of blackheads is compounds that can interact with the correlated with big pore size which makes dirt cytoplasmic membrane of the bacteria (Wijaya, or dust enter the skin easily. Aging and increase Napitupulu, Karnady & Indariani, 2018). in body temperature when doing exercise can lead to a bigger pore size in the skin. Therefore, Anti-Inflammatory Effect routine usage of PGM made from andaliman There is only one study available for the can be used as an alternative. andaliman anti-inflammatory effect. According Black spots formation is also one of the to a 2011 study, andaliman fruit extract was concerns related to skin aging. Black spots are capable of promoting the anti-inflammatory caused due to melanin production that is activity by suppressing the inflammatory induced by sunlight exposure. Flavonoid mediators such as TNF-α, IL-6, MMP9, COX-2 content in andaliman can help to decrease and iNOS in lipopolysaccharide (LPS)-induced melanin production by preventing tyrosine from macrophages. This study acted as in vitro cell becoming dihydroxyphenylalanine (DOPA) and model of gastric inflammation. The presence of DOPAquinone. Ethanolic extract of andaliman glycoprotein, phenylpropanoids, neolignan and containing flavonoids can reduce acne due to its alkaloids may contribute to the anti- antimicrobial activity and anti-inflammation inflammatory properties of andaliman (Yanti, which helps the recovery of the skin (Hanum & Nuriasari & Juliana, 2011). Laila, 2018).

Anti-aging and Anti-acne Anti-Halitosis Effect Aging can be defined as a condition where Halitosis is implied by bad smell from the the human body starts to lose their mouth due to the production of volatile sulphur physiological function which can be indicated by compounds (VSCs) by oral bacteria, and it is the decrease in reproductive rate (Flatt, 2012). mostly caused by lack of oral hygiene, Aging may also lead to the inability to respond periodontal infection, oral carcinoma, food towards stress conditions (Samarakoon, residues, and throat infection (Aylıkcı & Çolak, Ravishankar & Chandola, 2011). In most cases, 2013). A study by Yanti et al. (2019) determined people are being more concerned about skin the anti-halitosis effect of Z. acanthopodium aging. Skin aging can be caused by either essential oil (ZAEO) on inhibiting and removing intrinsic or extrinsic factors. Intrinsic factors biofilm plaque, reducing acid production, and such as genetic, hormones, and metabolism, inhibiting VSCs with Actinomyces viscosus while extrinsic factors are light exposure, model in vitro. The lowest dose used (20 ug/mL) pollution, radical, and toxins (Ganceviciene, of ZAEO in the experiment inhibited and Liakou, Theodoridis, Makrantonaki & Zouboulis, removed more than 50% of A. viscosus biofilms as well as total VSCs produced by the

12

Indonesian Journal of Life Sciences Vol. 02 | Number 01 | March (2020) http://journal.i3l.ac.id/ojs/index.php/IJLS/

microorganism. Consequently, the rapid essential oil and extracts of Zanthoxylum production of acid by A. viscosus was also alatum grown in North-Western inhibited by ZAEO in the concentration of 40 Himalaya. The Scientific World Journal, μg/mL. It is suggested that ZAEO extract could 2013. DOI: 10.1155/2013/790580 be administered as a natural ingredient for halitosis treatment (Yanti et al., 2019). Hanum, T. I., & Laila, L. (2016). Physical evaluation of anti-aging and anti-acne CONCLUSION Andaliman (Zanthoxylum acanthopodium Andaliman fruit might be used as an DC.) ethanolic extract peel off gel mask. ingredient in functional foods development Der Pharma Chemica, 8, 6-10. which has several health benefits such as Hartley, T. G. (1966). A revision of the Malesian antioxidant, antimicrobial, anti-inflammatory, species of Zanthoxylum (Rutaceae). anti-aging, anti-acne and anti-halitosis effects. Journal of the Arnold Arboretum, 47(3), Andaliman fruit is usually used for the making 171-221. of sambal sauce by the Batak tribe, Indonesia. In foods, andaliman is added to make Karnady, V. (2015). Comparison on in vitro Indonesian dishes such as arsik, tombur, and digestion effect of antioxidant and naniura. Moreover, its extract can also be antihyperglycemic activity from applied to fish and raw meat to prevent Andaliman (Zanthoxylum acanthopodium spoilage. DC.) and Japanese pepper (Zanthoxylum piperitum DC.) crude extract. Graduate REFERENCES Thesis, Bogor Agricultural University, Indonesia. Retrieved from Aylıkcı, B. U., & Çolak, H. (2013). Halitosis: From https://repository.ipb.ac.id/ diagnosis to management. Journal of Natural Science, Biology and Medicine, Kristanty, R. E., & Suriawati, J. (2014). Cytotoxic 4(1), 14. DOI: 10.4103/0976-9668.107255 and antioxidant activity of petroleum extract of Andaliman fruits (Zanthoxylum Flatt, T. (2012). A New Definition of Aging?. acanthopodium DC.). International Frontiers in Genetics, 3. DOI: Journal of PharmTech Research, 6(3), 10.3389/fgene.2012.00148 1064-1069. Ganceviciene, R., Liakou, A., Theodoridis, A., Muzafri, A., Julianti, E., & Rusmarilin, H. (2018). Makrantonaki, E., & Zouboulis, C. (2012). The extraction of antimicrobials Skin anti-aging strategies. Dermato- component of andaliman (Zanthoxylum Endocrinology, 4(3), 308-319. DOI: acanthopodium DC.) and its application 10.4161/derm.22804 on (Pangasius sutchi) fillet. IOP Guleria, S., Tiku, A. K., Koul, A., Gupta, S., Singh, Conference Series: Earth and G., & Razdan, V. K. (2013). Antioxidant Environmental Science, 122(1), p. and antimicrobial properties of the 012089). DOI :10.1088/1755- 1315/122/1/012089

13

Indonesian Journal of Life Sciences Vol. 02 | Number 01 | March (2020) http://journal.i3l.ac.id/ojs/index.php/IJLS/

Napitupulu, B., Simatupang, S., & Sinaga, M. Economic of Agriculture and Agribusiness, (2004). Potency of andaliman as a 2(4). additive of Batak ethnic North Sumatera. Seminar Nasional Siregar, B. L. (2003). Andaliman (Zanthoxylum Peningkatan Daya Saing Pangan acanthopodium DC.) di Sumatera Utara: Tradisional. Bogor, Indonesia. deskripsi dan perkecambahan. Hayati Journal of Biosciences, 10, 38-40. Nurlaeni, T & Junaedi, D. I. 2018. Studi ekologi habitat, teknik perbanyakan, dan Siregar, B. L. (2010). Upaya perbanyakan pengkoleksian dalam rangka konservasi andaliman (Zanthoxylum acanthopodium ex-situ andaliman (Zanthoxylum DC). Visi, 18(1), 17-28. acanthopodium DC). Bioma. 14(2), 80-88. Siregar, B. L. (2013). Perkecambahan dan Parhusip, A. J., Jenie, B. S. L., Rahayu, W. P., & pematahan dormansi benih andaliman Yasni, S. (2010). Effect of Andaliman (Zanthoxylum acanthopodium DC). Jurnal (Zanthoxylum acanthopodium DC) Agronomi Indonesia. 41(3), 249-254 extracts upon permeability and Sitanggang, F., Duniaji, A., & Pratiwi, I. (2019). hydrophobicity of Bacillus cereus. Jurnal Daya hambat ekstrak buah andaliman Teknologi dan Industri Pangan, 16(1), 24. (Zanthoxylum acanthopodium DC) dalam Purohit, S., Joshi, K., Rawat, V., Bhatt, I. D., & etil asetat terhadap pertumbuhan Nandhi, S. K. 2019. Efficient plant Escherichia coli. Jurnal Ilmu Dan regeneration through callus in Teknologi Pangan, 8(3), 257-266. Zanthoxylum acanthopodium DC : an Situmorang, P. C., Ilyas, S., Hutahaean, S., & endangered medicinal plant of the Indian Rosidah, R. (2019). Effect of nanoherbal Himalayan region. Plant Biosystems-An andaliman (Zanthoxylum acanthopodium) International Journal Dealing with all and extra virgin combination on Aspects of Plant Biology, 1-7. DOI: preeclamptic rats liver histology. The 10.1080/11263504.2019.1610107 Open Access Macedonian Journal of Samarakoon, S. M. S., Chandola, H. M., & Medical Sciences, 7(14), 2226. DOI: Ravishankar, B. (2011). Effect of dietary, 10.3889/oamjms.2019.651 social, and lifestyle determinants of Suryanto, E., Sastrohamidjojo, H., & Raharjo, S. accelerated aging and its common clinical (2004). Antiradical activity of andaliman presentation: A survey study. Ayu, 32(3), (Zanthoxylum acanthopodium DC) fruit 315. DOI: 10.4103/0974-8520.93906 extract. Indonesian Food and Nutrition Sibarani, R. V., Hutajulu, A. T., & Kusuma, S. I. Progress, 11(1), 15-19. DOI: (2013). Analisis pemasaran Andaliman 10.22146/jifnp.26 (Zanthoxylum acanthopodium DC) di Suryanto, E., Raharjo, S., Sastrohamidjojo, H., & Pasar Kota . Journal on Social Tranggono, T. (2005). Aktivitas

14

Indonesian Journal of Life Sciences Vol. 02 | Number 01 | March (2020) http://journal.i3l.ac.id/ojs/index.php/IJLS/

antioksidan dan stabilitas ekstrak International, 35(1), 1-19. DOI: andaliman (Zanthoxylum acanthopodium 10.1080/87559129.2018.1438470 DC) terhadap panas, cahaya fluoresen dan ultraviolet. agriTECH, 25(2), 63-69. Yanti, P. T., Nuriasari, N., & Juliana, K. (2011). Lemon pepper fruit extract (Zanthoxylum Hanum, T. I., & Laila, L. (2018). Evaluation of acanthopodium DC.) suppresses the anti-aging and anti-acne effect of expression of inflammatory mediators in andaliman (Zanthoxylum acanthopodium lipopolysaccharide-induced macrophages DcC) Ethanolic Extract Peel Off Gel Mask. in vitro. American Journal of Biochemistry Asian Journal of Pharmaceutical and and Biotechnology, 7(4), 190-5. DOI: Clinical Research, 11, 1-8. DOI: 10.3844/ajbbsp.2011.190.195 10.22159/ajpcr.2018.v11s1.26576 Yanti, Y., Gea, B. P., & Lay, B. W. (2019). Wijaya, C. H., Napitupulu, F. I., Karnady, V., & Antihalitosis effect of essential oil Indariani, S. (2019). A review of the extracted from Zanthoxylum bioactivity and flavor properties of the acanthopodium fruits. Jurnal Teknologi, exotic spice andaliman (Zanthoxylum 81(5). DOI: 10.1 acanthopodium DC.). Food Reviews

1113/jt.v81.13655|

15