Vol 4:19-26. Lactic acid fermentation of fish offal and chicken by-product with different starter cultures T. Mikael Lassén Division ofAnimal Nutrition, Department ofAnimal Science and Animal Health, Royal Veterinary and Agricultural University, Bulowsvej 13, DK-1870 Frederiksberg C, Denmark Lactic acid fermentation was evaluated as a method to preserve fish and chicken by-products. Her- ring ( Clupea harengus) by-products (viscera and heads) and chicken by-products (heads, viscera, feathers, feet and discarded whole chickens) were minced, mixed with 5% dextrose and inoculated with 108 colony forming units (cfu)/g of four different lactic acid bacteria cultures. The by-product was fermented at 25°C and evaluated for pH, % produced lactic acid, redox potential and odour during four weeks' storage. In herring offal, pH decreased from 6.8 to 4.2 in one week and stabilized at about 4.3. In the same time, 2.0% to 3.2% lactic acid was produced and concentrations stabilized from 2.5% to 4.0%. In chicken offal, pH decreased to a stable level of 4.4, and 3.2% lactic acid was produced after one week of fermentation. A negative and stable redox potential was achieved after one week of fermentation in both herring and chicken offal. Key words: animal waste, silage, lactic acid bacteria, redox potential, mink feed ntroduction Animal by-products are obtained in feed plants (pet food and fur animal feed) in which the raw material is processed in different ways, depend- ing on the origin and destinationof the feed. The most common processing methods are heating, drying, chilling and freezing. The increasing cost of energy has aroused interest in developing alternative storage meth- ods. Promising results have been obtained in preserving fish and slaughter-house by-products with lactic acid bacteria (LAB) (Kangas and Kangas 1983,Lindgren and Pleje 1983, Hassan and Heath 1986,Tibbets et al. 1987,Skrede and Nes 1988, Russel et al. 1992, Urlings 1992). Fermented silage is a product of a controlled fermentation process in which production of lac- tic acid (LA) results in a pH below 4.5. Owing to the lack of fermentable carbohydrates and a natural LAB flora, animal by-products cannot be subjected to lactic acid fermentation without the addition of a substrate. The methods used © Agricultural Science in Finland Manuscript received February 1994 19 AGRICULTURAL SCIENCE IN FINLAND https://www.c-info.fi/en/info/?token=NN8IpQd3ojD2PCvI.xhBoSfxMWDjJfEYRdU5WsQ.Me6m3alfv0gYSVXt8UQN4MSvX3YjsIgOX8LNBrWoxB9e9oFciICCEtZLk2NRcaiLB1f82I3P4RAyuguhDnELr1RIWbsdscvynmVgiCebrOn0uB8Vm6nt4baAk9c4qPntn07lNc9BzdTtzAgDwRIVbFQx9SjW9400JQyINrSlIaHRaEurhiVV9q8rk7thm--zFEOiVZViq5Z0G2SM8wuswf0_AxIoNYYAVh9N4p3ihgHN8fbD0q7VXQ8mP895FsC0RhK8ri6ZQVQ_v1tM Lassén, T. M.: Lactic acidfermentation offish offal and chicken by-product with different starter cultures are based on the addition of LAB and fermen- table carbohydrates to minced animal by-prod- ucts. The preservative action ofLAB in animal by- products is caused by low pH, a substantial amount of undissociated organic molecules, the buffering capacity of the raw material, hydro- gen peroxide production, competition with oth- er bacteria for nutrients, production of antibiot- ics and bacteriocines (bacteriocines are most often bacteriostatic to closely related species) and decreased redox potential (Raccach and Bak- er 1978, Smith and Palumbo 1981). The lower- ing in pH and the effect of undissociated LA in- hibit growth of bacteria such as Staphylococcus (Bartholomew and Blumer 1980), Escherichia coli (Tramer 1966), Serratia, Enterobacter, Cit- robacter, Achromobacter and Pseudomonas (Dubois et al. 1979). Bacteria strains commonly used as starter cultures are Lactobacillus plantarum (Kangas and Kangas 1983, Lindgren and Pleje 1983, Skrede and Nes 1988, Urlings 1992), Pediocco- cus acidilactici (Lindgren and Pleje 1983), Lactobacillus acidophilus (Tibbets et al. 1987) and some not fully characterized commercial cultures (Pelzyme®, Lassén et al. 1990a, b, PSI®, Russel et al. 1992, Stabisil®, Partanen et al. 1992). With a suitable starter culture, a mixture of fish or slaughter by-products and carbohy- drates may reach a pH of 4.4 to 5.0 in 24 to 48 h (Lindgren and Pleje 1983). Silage of this kind has been used as a component of feed for fur- bearing animals (Skrede and Nes 1988, Lassén et al. 1990a, b, Urlings 1992) and pigs (Tibbets et al. 1987, Partanen et al. 1992) with varying results. LAB fermentation ofanimal by-products may be worth developing as an alternative storage method, due to its economic advantages and its potential to kill pathogens (Wooley et al. 1981). To produce a quality feed product, the conditions for production from various raw materials have to be systematically evaluated, and efficient methods for quality control of the product de- veloped. This paper examines the conditions for fermentating herring and chicken offal. Material and methods Fish offal was fermented at the Royal Veterina- ry and Agricultural University, Denmark and chicken offal at FinnEwos Agri, Kariniemi, Fin- land. Fish offal (viscera and heads) from herring (Clupea harengus) caught in the North Sea in autum was obtained from Gilleleje Processing Plant, Gilleleje, Denmark. The offal was minced coarsely once through a 10-mm plate and deep- frozen within 6 h. The offal was kept at -20°C until 12h before it was to be used. All fermenta- tions were conducted using thawed herring of- fal, that had been mixed thoroughly in a Vari- mixer bakery machine and incubated at 25°C. Fermentation was conducted with commercial starter cultures containing Lactobacillus plantarum (L.p),Lactobacillus plantarum: Pedi- ococcus pentosaceus (L.p:P.p 1:2), Lactobacil- lus plantarum.Pediococcus acidilactici (L.p:P.a 1:2) (Chr. Hansen's Lab. A/S, Hprsholm, Den- mark), and the commercial Pelzyme® (Cultor Ltd., Feed Division, Helsinki, Finland). The her- ring offal was fermented for one week in 3-kg portions with 5% (w/w) dextrose added and an initial inoculum of 108 colony forming units (cfu)/g in 5 1 plastic containers equipped with a water airlock. After fermentation the material was stored at 25°C for four weeks. Chicken by-products were obtained from 39 day-old chickens and processed at the chicken slaughterhouse as follows. Immediately after slaughter of the chickens by-products (heads, viscera, feet and discarded whole chickens) were minced through a 10-mm plate, homogenized through a 6-mm plate and mixed with 12% (w/ w) extruded wheatmeal and feathers (2:1) ac- cording to the FinnEwos Agri method®; 5% dex- trose was then added. Finally, the starter culture was added when the material to be fermented had reached a temperature of 25°C. The same starter cultures were used as for fermentation of her- ring offal, with an initial inoculum of 108 cfu/g. All fermentations were conducted in triplicate at 25°C in the same types of plastic container as 20 AGRICULTURAL SCIENCE IN FINLAND Vol. 4: 19-26. used for herring offal. The fermented material was stored at 25°C for four weeks. Treatment effects were evaluated by moni- toring the pH values, LA production and chang- es in redox potential during four weeks of stor- age as previously described (Lassén 1995a). All three samples from each batch were analysed weekly for pH and LA production, and since earlier experiments (Lassén 1995a) had yielded very stable and reproducible results within treat- ments and time, only one sample per batch was measured for redox potential. Proximate analysis of herring and chicken offal before and after fermentation was conduct- ed according to standard methods. The dry mat- ter content was analysed by drying 4 g samples in a forced draught oven at 60°C for 18 h. Nitro- gen was determined by the Kjeldahl procedure and protein calculated as N x 6.25. Fat was hy- drolysed with HCI, extracted with petroleum ether and analysed by the Soxtec method. Solu- ble and hydrolysable hexose carbohydrates (dex- trose) were analysed according to Jacobsen (1981). Statistical analyses were performed accord- ing to the GLM procedure in SAS (SAS 1985). Changes in pH and LA production were evalu- ated separately for the fermentation of herring offal and chicken waste (1) and for the materi- als together (2) according to the following split- plot design model: Yi,» = |l + a. + b + c(i) + (ab),y + e.Jk where, Y k = the ijk th observation |i = general mean, a = fixed effect of starter culture,I ’ i = 1-4 (1) or material, i = 1 or 2 (2) b, = fixed effect of storage time ,j = 0,1, 2, 3 and 4 weeks (1 and 2), (ab)y = interaction effect between starter cul- ture, i = 1-4 (1), or material i = 1 or 2 (2) and storage time, 0-4 weeks (1 and 2), c (») = random sample within starter culture (1) or material (2), e... = random error.ijk Table I. LA-production and changes in pH in herring offal fermented with different startercultures, 10* cfu/g, and 5% dextrose, and chicken offal fermented with 5% dextrose and 12% extruded wheatmeal:feathers (2.1) and 108 cfu/g at 25°C. pH % LA Storage time, Herring Chicken Herring Chicken weeks 0 0.0 0.0 2.3* 3.2 b 2.8“ 4.1» 6.8 6.2 4.3 4.5 4,1 4.3 I 2 2.8* 4.1 b 2.4“ 4.0 b 3 4 4.2 4.4 4.4 4.4 a b Values differ significantly (PcO.Ol). LA= Lactic acid cfu = colony forming units Treatment effect were tested against the silo effect, thus using silos within starter culture (1) or material (2) as an error term. Results Fermentation of herring offal with 5% dextrose at 25°C resulted in a drop in pH from 6.8 to 4.3 (L.p) and from 6.8 to 4.0 (Pelzyme®), in one week; pH stabilized at between 3.9 and 4.5 after four weeks (Table 1). Rapid LA production was observed during the first week of fermentation, which stabilized at between 2% and 4% after four weeks of storage (Fig. la). The effect on redox potential showed a similar pattern, Pelzyme® having the most negative redox potential after four weeks (Fig. lb). Chicken offal was fermented successfully. Fermentation with 5% dextrose and 12% extrud- ed wheatmealrfeathers (2:1) resulted in rapid LA production (2.8% to 3.2%), and a pH drop from 6.2 to 4.4 in one week (Fig. 2a), followed by a negative redox potential (Fig. 2b). Pelzyme® re- sulted in a highly significant pH decrease 21 AGRICULTURAL SCIENCE IN FINLAND Lassén, T. M.: Lactic acidfermentation offish offal and chicken by-product with different startercultures (PcO.Ol) during the first week of fermentation, followed by stabilization at about pH 3.9. The other cultures tested were initially slower than Pelzyme®, but still showed a highly significant LA production and pH decrease after two weeks' storage. The difference in pH and LA produc- tion between the LAB cultures tested and Pelzyme® was significant (P<0.01) when herring offal was fermented, but no significance was noted between LAB cultures when chicken of- fal was used. Eventually a highly significant (p<0.01) difference in LA production between different materials was found for all cultures used in the present study; the pH decrease was, however, nonsignificant (Table 1). The freshly minced herring had the texture and appearance of coarsely minced fish, where- as the fermented offal was liquefied and had a clear layer of oil on the top. Chicken offal did not liquefy as much as herring offal during stor- age. In fermented herring and chicken offal the protein content in dry matter basis increased af- ter fermentation for one week. The offal did not contain fermentable carbohydrates before addi- tion of 5% dextrose (herring offal) and 12% ex- truded wheatmeal: feathers (2:1) and 5% dextrose (chicken offal), and only low concentrations (0.6% and 3.2%) remained after fermentation (Table 2). Conversion of dextrose/carbohydrates to LA was more effective in chicken offal than in her- ring offal (Fig. 3). In fermented herring offal, the decrease in dextrose did not, however, cor- respond with LA production, and only 40% to Fig. 1. Lactic acid fermentation of herring offal with different LAB cultures, 108 colony forming units/g and 5% dextrose at 25°C. a) Changes in pH, % LA. b)— Changes in redox potential. Fig. 2. Fermentation of chicken offal with different LAB cultures, 10Bcolony forming units/g, 5% dextrose and 12% extruded wheatmeal:feathers (2:1) at 25°C. a) —Changes in pH , % LA. b)— Changes in redox potential. 22 AGRICULTURAL SCIENCE IN FINLAND Vol. 4: 19-26. Table 2. Proximate composition of herring and chicken offal before and after fermentation for one week at 25°C. Offal DM Fat Protein Sugar Starch % % of DM %of DM % of DM % ofDM Herring” 29.3 38.6 35.4 14.6 0.0 Fermented herring 22.2 26.7 40.8 4.4 0.0 Chicken b 39.6 22.2 36.1 14.9 12.1 Fermented chicken 37.9 26.7 41.0 3.2 2.4 a Herring offal, 5% dextrose, and 10B cfu/g Lactobacillus plantarum b Chicken offal, 5% dextrose, 12% extruded whealmeal leathers (2:1), and 10*cfu/gLactobacillus plantarum cfu = colony forming units 45% of the dextrose was metabolized to LA with theLactobacillus plantarum-based cultures test- ed. Mainly in herring offal, when Pelzyme® was used as starter culture, the conversion of dex- trose to LA was 80% complete, and consequent- ly more acid was produced (Fig. la). Discussion Fast fermentation of herring offal with a rapid drop in pH to 4.4 or less resulted in a less putre- factive odour and a more stable silage than in silages produced at slower pH declines. In the literature, a preserving pH has been reported to occur after 24-72 h (Mackie et al. 1971, Raa 1980, Lindgren and Pleje 1983, Hassan and Heath 1986, Lassén et al. 1990a, b). Usually, a higher amount of lactic acid has to be produced in fish silage to yield a properly fermented prod- uct than in grass silage and silage from slaugh- ter-house wastes. Lindgren and Pleje (1983) found that the LA content giving a pH below 4.4 was above 4.0% in fish silage, about 3.0% in slaughter-house wastes and below 2.0% in grass silage. Hassan and Heath (1986) reported that 4.4% LA was needed to obtain a pH of 4.2 in fish silage fermented with 5% lactose as the car- bohydrate source. In the present study with its different starter cultures, 2.7% (L.p), 2.3% (L.p:P.p), 2.5% (L.p:P.a), and 2.5% (Pelzyme®) LA were needed to obtain a pH below 4.2, and 1.8% LA in fish silage resulted in a pH below 4.4, all concentrations being below the concen- trations reported in the literature. Successful fer- mentationof chicken offal was characterized by a higher initial lactic acid production to obtain a pH below 4.5; thus owing to its higher bone con- tent, chicken offal is likely to have a higher buff- ering capacity than herring offal. After three weeks' storage a minor drop in LA content was observed, possibly due to the hydrolysis of bone material, neutralizing the acid. This may also be followed by an accumulation of biogenic amines (Lassén 1995b), which also neutralized the ma- terial. A high LA concentration at pH 4.3 gives a high concentration of undissociated LA mole- cules; these provide the antimicrobial effect but Fig. 3. LA production from 5% dextrose for different LAB cultures (10* colony forming units/g) in silage made from herring and from 5% dextrose and 12% extruded wheatmeal:feathers (2:1)) in silage made from chicken of- fal at 25°C. 23 AGRICULTURAL SCIENCE IN FINLAND Lassén, T. M.: Lactic acid fermentation offish offal and chicken by-product with different starter cultures also inhibit further growth ofLAB (Baird-Park- er 1980). Measurements ofredox potential may be used to evaluate the growth conditions of anaerobic bacteria (Wolstrup 1972) and to determine the oxygen content of biological material (Harrison 1971). Lactobacilli are generally anaerobic to microaerophilic, demanding negative redox po- tentials, but certain strains grow aerobically and may lower the pH even under aerobic conditions (Kandler and Weiss 1986). Redox potential is always positive in the muscle and negative in the viscera of freshly caught herring (Huss and Larsen 1979). The redox potential in warm- blooded animals attains a negative value shortly after the animals have been slaughted and re- mains negative until aerobic deterioration sets in (Barnes and Ingram 1955, Wirth and Leistner 1970). Rapid establishment of the LAB is im- portant for LA production and the decrease in pH and redox potential. If the material reaches a low redox potential in a short time, growth of anaerobic bacteria, usually of the genera Al- teromonas, is inhibited. These bacteria are im- plicated in the spoilage of North Sea fish (Shewan 1977). Other bacteria of the genus Sal- monella are also known to be inhibited by a low redox potential (Chung and Goepfert 1970). Here, a low redox potential (-330mV to -680 mV) was achieved after one week of fermenta- tion, the level being somewhat lower for silage of herring offal than for silage of chicken offal. The results of this and an earlier study (Lassén 1995a) clearly show that appropriate fermenta- tion leads to a low and stable redox potential, whereas inappropriate fermentation leads to an increasing redox potential and pH as a result of decreased LA concentration. The more efficient use of dextrose as a car- bohydrate source when chicken offal was fer- mented might be explained by the lower number ofactively competing bacteria. Bacteria in chick- en have optimal growth conditions at about 30°C to 37°C, but fish bacteria are more active at lower temperatures (15°-25°C) and compete with LAB for free dextrose (Jay 1986). The changes record- ed in chemical content after fermentation were probably due to separation processes in the ma- terial, and were therefore considered not to re- flect true changes in chemical composition as an effect of the fermentation process. The de- creased fat content in dry matter after fermenta- tion might be explained by the separation proc- ess, in which the fat fraction is situated on top of the silo and the sample is taken from the bot- tom of the silo. The result of this study suggest that animal by-products can be fermented with 5% dextrose and 108 cfu LAB/g at 25°C, and that fermenta- tion is thus a viable alternative to current offal handling practices. Successful fermentation de- pends, however, on the hygienic quality of the raw material and good hygiene at the process- ing plant. To improve the process, there is still a need for development of better starter cultures and methods for determining product quality. Acknowledgements. Financial support was provided by the Academy of Finland. My sincere gratitude is due to Mrs Birthe lessen of Chr. Hansen's Lab., A/S, Hprsholm, Den- mark, for providing the starter cultures and for her valua- ble suggestions on which cultures touse, to Mr Matti Laiti- nen of Cultor Ltd, Helsinki, Finland and to Mr Karl-Erik Forsman of FinnEwos Agri, Vaasa, Finland, for assistance with chicken offal fermentation, to Associate Professor Anne-Helene Tauson for constructive criticism, and for her skilful help with statistical analysis, and to Associate Pro- fessor Niels Enggaard Hansen forvaluable suggestions and comments. References Baird-Parker, A. C. 1980. Organic Acids. In: Silliker, J. dation-reduction potential of the sterno-cephalicus mus- H. (ed ). Microbial Ecology of Foods. Vol. 1. Academic cle of the horse after death in relation to the develop- Press, London, p. 126-135. ment of bacteria. Journal of the Science of Food and Barnes, E. M. & Ingram, M. 1955. Changes in the oxi- Agriculture 6: 448-455. 24 AGRICULTURAL SCIENCE IN FINLAND Vol 4: 19-26. Bartholomew, D. T. & Blumer, T. N. 1980. 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Wooley, R. E„ Gilbert, T. P„ Whitehead, W. K., Shotts, E. B. Jr. & Dobbins, C. N. 1981. Survival of viruses in fermented edible waste material. American Journal of Veterinary Research 42: 87-90. 25 AGRICULTURAL SCIENCE IN FINLAND Lassén, T. M.: Lactic acidfermentation offish offal and chicken by-product with different starter cultures SELOSTUS Kala- ja kanajätteiden maitohappofermentaatio erilaisilla mikrobiviljelmillä T. Mikael Lassén Royal Veterinary and Agricultural University , Tanska Tutkimuksessa selvitettiin, soveltuuko maitohap- pofermentaatio kala-ja kanajätteiden säilömismene- telmäksi. Sillin {Clupea harengus) jätteet (sisälmyk- set ja päät) ja kanajätteet (päät, sisälmykset, höyhe- net, jalat ja hylätyt kokonaiset kanat) hienonnettiin, sekoitettiin 5 %:een dekstroosiin ja siirrostettiin nel- jään erilaiseen I0 K cfu/g maitohappobakteeri viljel- mään. Tätä sivutuotetta fermentoitiin 25 °C lämpö- tilassa. pH, maitohappopitoisuus %, redox-potenti- aali ja haju tutkittin neljän viikon varastointiaikana. Sillijätteen pH laski 6,B:sta 4,2:een viikossa ja vakiintui 4,3:een. Samanaikaisesti maitohappopitoi- suus oli 2,0 % - 3,2 % ja pitoisuudet vakiintuivat 2,5 %:sta 4,0 %:iin. Kanajätteen pH laski ja vakiin- tui 4,4:ään, ja maitohappopitoisuus oli 3,2 % viikon fermentaation jälkeen. Sekä silli- että kanajätteellä oli negatiivinen ja vakaa redox-potentiaali viikon fer- mentaation jälkeen. 26 AGRICULTURAL SCIENCE IN FINLAND