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Effect of fuel and kiln type on the polycyclic aromatichydrocarbon (PAH) levels in smoked shrimp, aBeninese food condimentEuloge Yénoukounmè Kpocloua, Victor Bienvenu Anihouvia, Paulin Azokpotaa, MohamedMansourou Soumanoub, Caroline Dounyc, François Brosec, Djidjoho Joseph Hounhouigana &Marie-Louise Scippoc

a Department of Nutrition and Food Science, Faculty of Agronomic Sciences, University ofAbomey-Calavi, Cotonou, Beninb Polytechnic School of Abomey-Calavi, University of Abomey-Calavi, Cotonou, Beninc Department of Food Science, Faculty of Veterinary Medicine, University of Liège, Liege,BelgiumAccepted author version posted online: 24 Apr 2014.Published online: 28 May 2014.

To cite this article: Euloge Yénoukounmè Kpoclou, Victor Bienvenu Anihouvi, Paulin Azokpota, Mohamed MansourouSoumanou, Caroline Douny, François Brose, Djidjoho Joseph Hounhouigan & Marie-Louise Scippo (2014): Effect of fuel andkiln type on the polycyclic aromatic hydrocarbon (PAH) levels in smoked shrimp, a Beninese food condiment, Food Additives& Contaminants: Part A, DOI: 10.1080/19440049.2014.916422

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Effect of fuel and kiln type on the polycyclic aromatic hydrocarbon (PAH) levels in smokedshrimp, a Beninese food condiment

Euloge Yénoukounmè Kpocloua, Victor Bienvenu Anihouvia, Paulin Azokpotaa, Mohamed Mansourou Soumanoub,Caroline Dounyc, François Brosec, Djidjoho Joseph Hounhouigana* and Marie-Louise Scippoc

aDepartment of Nutrition and Food Science, Faculty of Agronomic Sciences, University of Abomey-Calavi, Cotonou, Benin; bPolytechnicSchool of Abomey-Calavi, University of Abomey-Calavi, Cotonou, Benin; cDepartment of Food Science, Faculty of Veterinary Medicine,University of Liège, Liege, Belgium

(Received 11 March 2014; accepted 15 April 2014)

Smoked shrimp is a food condiment widely used in Beninese local cooking practices. A previous study revealed that thisproduct is highly contaminated with polycyclic aromatic hydrocarbons (PAH). The present study explored possibilities toreduce PAH levels in shrimp smoked using cottage industry smoking techniques with barrel and chorkor kilns, by replacingwood by charcoal from Acacia auriculiformis and Mangifera indica, as fuels. Results showed that only shrimp smokedusing acacia charcoal in a chorkor kiln had PAH levels (benzo[a]pyrene = 5 µg kg−1 and sum of benzo[a]pyrene, chrysene,benzo[a]anthracene and benzo[b]fluoranthene = 28 µg kg−1) in accordance with a European standard of 5 and 30 µg kg−1,respectively, and suitable physicochemical characteristics for good storage (moisture content = 11.9% ± 1.5%; wateractivity = 0.46 ± 0.03). However, further investigations still needs to be done to reduce the duration of product contactwith combustion gasses in order to reduce the PAH content of smoked shrimp to safer levels, largely below standards.

Keywords: shrimp; smoking; food condiment; kiln; polycyclic aromatic hydrocarbon (PAH)

Introduction

Food self-sufficiency is an important challenge for the devel-opment of every nation. However, more than food availabil-ity, food quality becomes worrying as regards the diversity offood-borne diseases. As well as the quality of the rawmaterial, processing technology is critical in determiningthe quality of final products. In many costal countries inWest Africa the smoking process is the most used methodfor the reduction of post-harvest loss of fish. Apart fromassuring a longer shelf-life, smoking gives the product adesirable colour, taste and odour (Olley et al. 1988; Clucas& Ward 1996; Horner 1997; Eyo 2001; Sengor et al. 2004;Olokor et al. 2007). However, cottage industry food smokingis recognised as a food processing method leading to foodcontamination with chemical hazards (SCF 2002; CCFAC2005; Moret et al. 2005; Yurchenko & Mölder 2005).Cottage industry food smoking is made in kilns and involvesprocessing with wood smoke produced by smouldering cer-tain wood (varying according to the locality), their shavings,sawdust or charcoal. The fuel is put directly below thehanging fish or the fish is spread on mesh trays. Duringwood smouldering, toxic chemical compounds can beformed, mainly polycyclic aromatic hydrocarbons (PAHs)(Gomaa et al. 1993; Yabicu et al. 1993; Akpan et al. 1994;Garcıa Falcon et al. 1996; Moret et al. 1999; Pagliuca et al.2003). PAHs are generally classified as relatively persistentorganic environmental contaminants (Harvey 1997; Martson

et al. 2001; Deshpande 2002). Several PAHs have beenfound to induce a number of adverse effects such as immu-notoxicity, genotoxicity and mutagenicity (EFSA 2008;IARC 2010; Sánchez-Guerra et al. 2012). Benzo(a)pyrene,maybe the most known congener of the PAH family, isclassified as carcinogenic for human (class 1) (IARC 1983).

In food, according to the Regulation (EC) No. 1881/2006,maximum levels existed only for benzo(a)pyrene (BaP) (until2012) for a limited category of foods. A recent risk assessmentperformed by EFSA showed that four PAHs are relevantaccording to both their occurrence in food and their toxicity.This list, so-called ‘PAH4’, includes BaP, chrysene (CHR),benzo[a]anthracene (BaA) and benzo[b]fluoranthene (BbF)(EFSA 2008). Subsequently, Regulation (EC) No. 1881/2006 was modified to include two kinds of maximum levelsfor PAHs in food, one for BaP and one for the sum of thePAH4, valid from 1 September 2012. For smoked crustaceans,these limits are 5 and 30 µg kg−1, respectively, until 31 August2014, and 2 and 12 µg kg−1 respectively from 1 September2014 (EC 2011).

In Benin, smoked shrimp is a food condiment mostlyused in local cooking practices. Traditionally, shrimps aresmoked in a barrel or chorkor kiln with wood as fuel, for 5–8 h, in order to lower the water activity and to improve theirshelf-life (10–24 weeks) (Degnon et al. 2013). A previousstudy showed that shrimps smoked using cottage industryprocessing methods are highly contaminated with PAH,

*Corresponding author. Email: joseph.hounhouigan@gmail.com

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showing BaP and sum of PAH4 contents of 91 and 490 μgkg−1 respectively, i.e. about 30 times higher than theEuropean maximum limits (Kpoclou, Anihouvi, Azokpota,et al. 2013). Used as a condiment, this product can beconsumed with many foods. Therefore, smoked shrimpscan be considered as a potential vehicle for exposure tocarcinogenic compounds. The present study explored possi-bilities for reducing PAH levels in shrimp smoked usingcottage industry techniques (i.e. in barrel and chorkorkilns). With this aim, the wood, which is the fuel usuallyused to produce smoke, was replaced by charcoal fromAcacia auriculiformis and Mangifera indica.

Material and methods

Smoking experimentation

Wild fresh shrimps (Penaeus duorarum) of size of 76–80pieces/kg from Nokoué lake were obtained from fisher-men. Processing was carried out according to traditionalpractices by hot smoking in two types of kilns, chorkorand barrel, which are the most used kilns by producers(Degnon et al. 2013). The chorkor kilns were constructedfrom bricks as described by Diakite (1988); the barrelkilns were of iron, as described by Idah & Nwankwo(2013) using the dimensions summarised in Table 1.

Two types of fuel obtained from two kinds of treewere used, charcoal and wood from A. auriculiformis(8% and 23% moisture content respectively) and M. indica(9% and 10% moisture, respectively). A. auriculiformiswood is the most used fuel in cottage industry smokingunits in Benin (45% of processors) (Kpoclou, Anihouvi,Scippo, et al. 2013); while M. indica wood was chosenbecause it is less rich in lignin than all the other woodsused as fuel in shrimp smoking, according to guidelinesfrom CAC (2009). Smoking was achieved with 5 kg ofshrimp for each smoking trial. The temperature was mon-itored in the fuel in combustion and in the mass of theproduct undergoing the smoking process, at 30-min inter-vals, using a thermometer (Thermocouple TSTEMP 10 K,Oakton, Singapore). Each fuel was used individually ineach kind of kiln. Each trial was repeated three times withthree producers and the end of smoking was based on theknow-how of the producer, on the basis of the colour andthe dryness of the shrimp. In total, 24 batches of smoked

shrimps were produced, and shrimp samples were col-lected for analysis.

Analysis

Moisture content and water activity (aw)

The moisture content was determined by oven drying of5 g of grinded shrimp at 105°C until a constant weightwas reached (AOAC 1995). Water activity (aw) was mea-sured according to the method described by Anihouviet al. (2006) using a thermo-hygrometer recorder(Rotronic HygroLab 2, Bassersdorf, Switzerland).

Polycyclic aromatic hydrocarbons determination

The collected raw and smoked shrimps samples wereanalysed for PAH content according to the proceduredescribed by Kpoclou, Anihouvi, Azokpota, et al.(2013). After lyophilisation of samples, 1 g of freeze-dried shrimp sample was extracted with hexane/acetone(50:50, v/v) using the accelerated solvent extraction (ASE)technique. The solvent was evaporated until 1 ml andreconstituted with 5 ml of cyclohexane. The reconstitutedextract was purified by column chromatography usingEnviChrom P column (Supelco) conditioned successivelywith 15 ml ethyl acetate and 10 ml cyclohexane. Afterloading the sample extract, the column was washed with6 ml cyclohexane/ethanol (70:30, v/v) and PAHs wereeluted using 12 ml of cyclohexane/ethyl acetate (40:60,v/v) (Veyrand et al. 2007). The solvent was evaporateduntil dryness. The final extract was reconstituted with90 µl acetonitrile and then spiked with 10 µl of deuteratedDiP (internal standard). A total of 5 µl of this final extractwas analysed by HPLC coupled to a fluorescence detector(HPLC/FLD), according to Brasseur et al. (2007) andDanyi et al. (2009). The analysis was carried out using aModel 600 E solvent delivery system equipped with aModel 717 automatic injector, a MistralTM oven andboth 996 PDA and 2475 fluorescence detectors (allWaters). A C18 Pursuit 3 PAH (100 × 4.6 mm, 3 µm)equipped with a ChromGuard (10 × 3 mm) pre-column,both from Varian, was used to separate the PAHs. Forsmoked shrimp (with low moisture content), the LOQsof the method were 0.85 µg kg−1 for benzo(j)fluorantheneand indeno[123-cd]pyrene and 0.21 µg kg−1 smokedweight for all the other PAHs, while for raw shrimp(with a high moisture content) the LOQs were 0.06 and0.25 µg kg−1 respectively. The expanded measurementuncertainty was estimated to 20%.

Statistical analysis

Statistical analysis was performed using Statistical pack-age for the Social Sciences (SPSS, version 16). Data are

Table 1. Dimensions (cm) of kilns used for the experiments.

Body of the kiln Opening

Height ThicknessInternaldiameter Base Height

Chorkor kiln 46–52 23–26 64–70 44–45 36–40Barrel kiln 45–48 0.1 56–65 35–43 22–29

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presented as mean and standard deviation; significancewas set at p < 0.05 and means were separated usingSNK (Student, Newman and Keuls) range test.

Results and discussion

Evolution of temperature during smoking process

Figure 1 shows the evolution of temperature in the fuelin combustion and in the mass of shrimps from thebeginning to the end of the smoking process. In chorkorkiln (Figure 1a), the temperature of wood increasedfrom 558°C (t = 0 min) to 707°C (t = 60 min) anddecreased progressively to 442°C (210 min). The tem-perature of charcoal increased from 465°C (t = 0 min)to 627°C (t = 60 min) and decreased progressively to450°C (t = 210 min). In shrimp, data showed that whensmoking was achieved with wood, temperature in massof shrimp increased from 34°C (t = 0) to 91°C(t = 90 min) and decreased progressively to 66°C(t = 210 min). During the smoking with charcoal, tem-perature in mass of shrimp increased from 34°C(t = 0 min) to 89°C (t = 120 min) and decreased to

55°C (t = 210 min). When the smoking was achievedusing barrel kilns, the evolution of the temperatures inboth fuel and shrimp was roughly the same as the onerecorded in chorkor kiln smoking conditions (Figure1b). Likewise, evolution of the temperatures in bothfuel and shrimp was approximately the same when thesmoking was achieved using magifera indica (data noshown).

Smoking process with the chorkor kiln lasted210 min (Figure 1a) while it took longer (300 min) toachieve the smoking of shrimps using barrel kilns(Figure 1b). The shorter processing time needed whenusing chorkor kilns is because these kilns are built withbricks of clay of thickness of 23–25 cm, and no loss ofheat occurs from fuel burning through the kiln. Figure1a and 1b showed that the temperature in the mass ofshrimp was above 70°C at least for 1 h during smoking,in the four conditions tested. Therefore, traditionalsmoking can be assimilated to pasteurisation, meaningthat the temperature attained in shrimp during smokingis sufficient to eliminate Gram-negative bacteria such asPseudomonas, Escherichia coli and Salmonella as noti-fied by Plahar et al. (1999).

Figure 1. Evolution of temperature in fuel and shrimp during the smoking process: (a) smoking in a chorkor kiln (n = 3); and (b)smoking in a barrel kiln (n = 3).

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Physicochemical characteristics of shrimps aftersmoking process

Moisture content and water activity (aw)

Table 2 shows the moisture content and the water activity ofboth raw and smoked shrimps. The moisture content insmoked shrimps was five to seven times lower than in rawshrimp (11.9–14.6% and 79.1%, respectively) while thewater activity (Aw) was significantly (p < 0.05), reducedfrom 0.93 in raw shrimp to around 0.50 in smoked shrimp.Salan et al. (2006) and Kumolu-Johnson et al. (2009)reported that spoilage of fish resulting from the action ofenzymes and bacteria can be slowed down by the reductionin moisture through smoking. The value of water activityattained in smoked shrimp were lower than 0.7, an aw levelbelow which bacterial growth would be impossible in foodproducts (Prescott et al. 2003). These values of moisturecontent and water activity are similar to those measured insmoked shrimp collected in local market in Benin (moisture:14.0% and aw: 0.6) by Kpoclou, Anihouvi, Azokpota, et al.(2013). Thus, shrimp smoking achieved in the present studyreflects usual practices of producers, regarding moisturecontent and aw of the final product.

Polycyclic aromatic hydrocarbons’ (PAHs) content

PAH content in raw and smoked shrimp as a function ofthe fuel and the kiln used is summarised in Tables 3 and 4respectively. Data showed that PAHs contents were presentin raw shrimp only in traces amounts (Table 3). In smokedshrimp obtained by smoking in chorkor kiln, PAH averagecontent of 5 µg kg−1 (BaP) and 28 µg kg−1 (sum of PAH4)were recorded when smoking was achieved with acaciacharcoal, while 107 µg kg−1 (BaP) and 394 µg kg−1 (sumof PAH4) were found when wood was used (Table 4).When smoking was achieved in barrel kiln using acaciacharcoal, PAH content in shrimp was 13 µg kg−1 for BaPand 71 µg kg−1 for the sum of PAH4, while 92 µg kg−1

and 482 µg kg−1 were recorded respectively when woodwas used (Table 4). The same tendencies were observedwhen smoking was performed with mango tree charcoaland wood both in chorkor and barrel kilns (Table 4).

The temperature of fuel during combustion is animportant factor for PAH formation. Moret et al. (1999)and Visciano et al. (2008) reported that during smoking,PAHs are formed and migrate easily toward the innertissue of fish. Furthermore, it was shown that, duringsmoking processes, PAH begin forming when temperatureof fuel combustion exceeds 450°C (Stołyhwo & Sikorski2005; Ravindra et al. 2008). This temperature conditionwas met in this study, since in all smoking conditionstested, the temperature of fuel combustion was above450°C from 0 to 180 min (Figure 1a and 1b). In barrelkilns with wood, the temperature of fuel burning remainedeven longer above 450°C, from 0 to 240 min (Figure 1b).

Another important factor for the PAH formation is theheat source. This study showed that PAH levels vary withthe nature of the fuel. In this study, the acacia wood is farmore humid (23%) than the mango wood (10%). Thishigher humidity could have resulted in more smoke andtherefore possibly explained the higher levels of PAHsfrom acacia wood as shown in Table 4. A supplementaryexperiment using mango and acacia woods at the samehumidity could help to determine the intrinsic potential of

Table 2. Moisture content and water activity (aw) of raw and smoked shrimps.

Sample Kiln type Fuel type Moisture (%) Aw

Raw shrimp (n = 4) − – 79.1 ± 1.3a 0.93 ± 0.01a

Acacia charcoal 11.9 ± 1.5c 0.46 ± 0.03b

Chorkor kiln (n = 3) Mango tree charcoal 12.5 ± 0.1bc 0.52 ± 0.00bcd

Acacia wood 13.4 ± 0.7bc 0.49 ± 0.03bc

Smoked shrimp Mango tree wood 13.7 ± 1.1bc 0.60 ± 0.05d

Acacia charcoal 14.0 ± 1.6bc 0.54 ± 0.06bcd

Barrel kiln (n = 3) Mango tree charcoal 12.7 ± 1.6bc 0.48 ± 0.06b

Acacia wood 14.3 ± 1.0bc 0.53 ± 0.04bcd

Mango tree wood 14.6 ± 0.1b 0.57 ± 0.05cd

Note: *Mean ± standard deviation; a, b, c and dvalues in the same column followed by different letters are significantly different (p < 0.05).

Table 3. PAH content (µg kg−1) (mean ± standard deviation) inraw shrimp used for smoking trials (n = 4).

PAH LOQ Content

Benzo[b]fluoranthene (BbF) 0.06 0.07 ± 0.02Dibenzo[a,l]pyrene (DlP) 0.06 < LOQDibenzo[a,h]anthracene (DhA) 0.06 < LOQBenzo[ghi]perylene (BgP) 0.06 < LOQDibenzo[a,e]pyrene (DeP) 0.06 < LOQBenzo[j]fluoranthene (BjF) 0.25 < LOQBenzo[c]fluorene (BcL) 0.06 0.12 ± 0.02Benzo[a]anthracene (BaA) 0.06 0.09 ± 0.03Chrysene (CHR) 0.06 0.14 ± 0.045-Methylchrysene (5MC) 0.06 < LOQBenzo[k]fluoranthene ( BkF) 0.06 < LOQBenzo[a]pyrene (BaP) 0.06 < LOQIndenol[1,2,3-cd]pyrene (IcP) 0.25 < LOQDibenzo[a,i]pyrene (DiP) 0.06 < LOQDibenzo[a,h]pyrene (DhP) 0.06 < LOQ

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each wood type to generate PAHs during smoking. Eitherwith the chorkor or the barrel kiln technique, the PAHlevel in smoked shrimp was much higher when smokingwas performed with wood than with charcoal. This is dueto the fact that charcoal has been obtained from previoussmouldering of wood. This previous burning of woodreduces the quantity of precursors available for PAHsynthesis reaction. Furthermore, charcoal combustion gen-erates low amount of smoke and does not produce flame,while wood burning generates high amount of smoke andproduces some flame (Silva et al. 2011). Lijinsky (1991)and Rey Salgueiro et al. (2004) have demonstrated that thelevels of PAH in the smoke increased when the materialswere burnt with flames. In this study, the higher level ofPAH in smoked shrimp from smoking with firewood inthe two types of kilns would be associated with the flameproduced during smouldering.

Smoking in chorkor kiln with acacia charcoal resultedin 5 µg kg−1 (BaP) and 28 µg kg−1 (sum of PAH4) inshrimp, against 14 µg kg−1 (BaP) and 92 µg kg−1 (sum ofPAH4) with mango tree charcoal. The values obtainedwith acacia charcoal are in accordance with the specifiedvalues in the European regulation, valid until 31 August2014 (Regulation (EU) No. 835/2011), 5 µg kg−1 (BaP)and 30 µg kg−1 (sum of HAP4). Smoking in barrel kilnwith charcoal resulted in higher levels of PAH (13 µg kg−1

(BaP) and 71 µg kg−1 (sum of PAH4) with acacia charcoaland 11 µg kg−1 (BaP) and 54 µg kg−1 (sum of PAH4) withmango tree charcoal), probably because of the longerprocessing (300 min instead of 210 min in chorkorkilns), leading to more than twice the European maximumlimits. In respect to the European standard, smoking inchorkor kiln with acacia charcoal appears to be the bestpractice to ensure safety levels of PAH in smoked shrimps.

Conclusion

From fuel–kiln combinations tested in this study, onlysmoking with acacia charcoal in chorkor kiln led to asafe product regarding its PAH contamination, with levels

below current maximum European Union limits, whereassmoking shrimp with wood greatly exceeds EuropeanUnion limits. However, these levels (5 µg kg−1 (BaP)and 28 µg kg−1 (sum of PAH4)) should be reduced further,because they are still too high to meet the future maximumlimits of 2 and 12 µg kg−1 respectively stipulated byRegulation (EC) No. 1881/2006 (EC 2011) to applyfrom September 2014. More studies must be done toreduce the duration of shrimp contact with combustiongases and to explore different types of wood, in order toproduce good-quality smoked shrimp and to ensure thesafety of Beninese consumers.

AcknowledgementsThis paper is part of the PhD work for the first author.

FundingFinancial support for this work was received from the BelgiumGovernment through the UAC 01 Project. The authors are verygrateful for this support.

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