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Quantitative Microbiology
in Food Processing
Quantitative
Microbiology
in Food Processing
Modeling the Microbial Ecology
Edited by

Anderson de Souza Sant’Ana

Department of Food Science,
University of Campinas, Brazil
This edition first published 2017 © 2017 John Wiley & Sons, Ltd.
Registered Office
John Wiley & Sons, Ltd, The Atrium, Southern Gate, Chichester, West Sussex, PO19 8SQ, UK
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10 9 8 7 6 5 4 3 2 1
Contents

List of contributors, xvi

Part I Introductory section, 1

1 Introduction to the microbial ecology of foods, 3
D. Roy and G. LaPointe
1.1 Introduction, 3
1.2 Role of food characteristics and environment on microbial fate, 4
1.2.1 Temperature, 4
1.2.2 pH and acidity, 5
1.2.3 Water activity, 6
1.2.4 Oxygen and redox potential, 6
1.2.5 Nutrient content, 7
1.2.6 Physical structure and microenvironments, 7
1.2.7 Food preservation processes (antimicrobials, preservatives), 7
1.3 Understanding microbial growth, death, persistence, competition, antagonism
and survival in food, 8
1.3.1 Principles of microbial growth, 8
1.3.2 Survival, 8
1.3.3 Strategies for persistence, 9
1.3.4 Competition, 9
1.4 Methods to study the microbial ecology of foods, 11
1.4.1 Culture‐independent analysis of microbial communities, 11
1.5 Perspectives on applying food ecosystem modeling, 12
References, 13
2 Predictive microbiology: mathematics towards understanding the fate of food‐borne
microorganisms in food processing, 16
P.N. Skandamis and E.Z. Panagou
2.1 Introduction, 16
2.2 Probability and kinetic models for food processing and HACCP, 18
2.2.1 Probability of growth models, 18
2.2.2 Growth kinetic models, 24
2.3 Thermal inactivation, 32
2.4 Non‐thermal inactivation and modeling stress‐adaptation strategies, 34
2.4.1 Modeling the adaptive responses of pathogens to inimical factors, 36
2.5 Fermentation: a dynamic environment for microbial growth and pathogen inactivation, 38
2.6 Colonial versus planktonic type of growth: modes of microbial existence on surfaces
and in liquid, semi‐liquid, and solid foods, 41
2.6.1 Biofilm formation on biotic and abiotic surfaces, 41
2.6.2 Growth rate of microorganisms in different forms of growth, 42

v
vi   Contents

2.7 Modeling microbial transfer between processing equipment and foods, 45

2.8 Alternative multivariate approaches: the use of bioinformatics for characterizing spoilage
and product classification, 49
References, 51
3 Principles of unit operations in food processing, 68
A. Ibarz and P.E.D. Augusto
3.1 Introduction, 68
3.2 Principles of transport phenomena, 68
3.3 Principles and unit operations of momentum transfer, 69
3.3.1 Food rheology, 69
3.3.2 Fluid flow, 71
3.3.3 Pumping and mixing, 72
3.4 Principles and unit operations of heat transfer, 73
3.4.1 Absorbing or removing thermal energy, 73
3.4.2 Heat transfer mechanisms and process conditions, 74
3.4.3 Steady state heat transfer, 75
3.4.4 Unsteady state heat transfer, 76
3.4.5 Heat transfer in the thermal process, 78
3.5 Principles and unit operations of mass transfer, 81
3.5.1 Mass transfer mechanisms, 81
3.6 Conclusions, 82
References, 83

Part II Impact of unit operations on microorganisms of relevance in foods, 85

4 Impact of materials handling at pre‐ and post‐harvest operations on the microbial ecology
of foods of vegetable origin, 87
A.N. Olaimat, P.J. Delaquis, and R.A. Holley
4.1 Introduction, 87
4.2 The production environment, 90
4.3 Soil, 91
4.4 Fertilizers derived from animal wastes, 92
4.5 Irrigation, 93
4.6 Harvesting and handling, 98
4.7 Postharvest processing, 99
4.8 Packaging, storage, and transportation, 101
4.9 Conclusions, 103
References, 103
5 Impact of heating operations on the microbial ecology of foods, 117
E. Xanthakis and V.P. Valdramidis
5.1 Background and basic information of heating operations, 117
5.1.1 Cooking (grilling, broiling, griddle, roasting, frying, stewing, sous‐vide, braising), 117
5.1.2 Blanching, 120
5.1.3 Pasteurization, 121
5.1.4 Commercial sterilization, 122
5.1.5 Ohmic heating, 123
 Contents   vii

5.1.6 Dielectric heating, 125

5.1.7 Infrared heating, 130
5.2 Quantitative aspects and how unit operations impact on food‐borne microorganisms, 131
5.3 Application of F‐value concept, 132
5.4 Dealing with non‐linearity, 133
5.5 Development of new concepts to assess heat processes, 135
5.6 Microbial safety and stability of heating operations: challenges and perspectives, 136
References, 136
6 Impact of refrigeration operations on the microbial ecology of foods, 142
L. Huang
6.1 Introduction, 142
6.2 Refrigeration as a unit operation, 143
6.2.1 Basic principles of refrigeration, 143
6.2.2 Changes in the microorganisms during freezing, 144
6.2.3 Changes in the microorganisms during refrigerated storage, 145
6.3 Dynamic effect of chilling on growth of C. perfringens during cooling, 147
6.3.1 Mathematical modeling of growth of C. perfringens during cooling, 148
6.3.2 Effect of temperature on growth of C. perfringens during cooling – secondary
model, 148
6.3.3 Prediction of growth of C. perfringens during cooling – a finite element
analysis, 149
6.3.4 Heat and mass transfer during heating and cooling, 149
6.3.5 Finite element analysis, 150
6.3.6 Computer simulation of transient temperature changes during cooling, 152
6.3.7 Integration of heat transfer and growth kinetics to simulate dynamic growth
of C. perfringens during cooling, 155
6.3.8 Conclusion and impact on growth of C. perfringens during cooling, 157
References, 158
7 Impact of dehydration and drying operations on the microbial ecology of foods, 160
F. Pérez‐Rodríguez, E. Carrasco, and A. Valero
7.1 Introduction, 160
7.2 Modeling the drying process in food, 161
7.3 Modeling microbial survival/inactivation in drying/dehydration processes, 163
7.3.1 Overview, 163
7.3.2 Primary models at static conditions, 164
7.3.3 Linear and non‐linear inactivation kinetics at dynamic conditions, 166
7.3.4 Secondary models, 167
7.3.5 Survival/inactivation of microorganisms in low‐moisture foods, 168
7.4 Example of application/development of predictive microbiology models for describing
microbial death during drying processes, 169
7.4.1 Listeria monocytogenes inactivation as a function of temperature
and aw, 169
7.4.2 Salmonella inactivation during drying of beef jerky, 171
7.4.3 Salmonella inactivation during drying of sausages, 172
7.5 Conclusions, 173
References, 173
viii   Contents

8 Impact of irradiation on the microbial ecology of foods, 176

S. Unluturk
8.1 Introduction, 176
8.2 Ionizing radiation, 176
8.2.1 Impact of ionizing radiation on food‐borne microorganisms, 177
8.3 Non‐ionizing radiation, 180
8.3.1 Impact of non‐ionizing radiation on food‐borne microorganisms, 181
References, 187
9 Impact of high‐pressure processing on the microbial ecology of foods, 194
S. Mukhopadhyay, D.O. Ukuku, V. Juneja, and R. Ramaswamy
9.1 Introduction, 194
9.2 Processing operation, 195
9.3 Bacteria and enzyme inactivation, 195
9.4 Effect of high pressure on fruit and vegetable products, 198
9.5 Effect of HHP on meat and other food products, 198
9.6 Effect of added antimicrobial on pathogen inactivation by high‐pressure processing
(hurdle approach), 199
9.7 High‐pressure carbon dioxide (HPCD) disinfection, 200
9.8 Effect of HHP on bacteria, virus, insects, and other organisms, 201
9.9 Effect of HHP on quality: color, flavor, texture, sugar, totally soluble, and insolubles, 203
9.10 Advantages and disadvantages of using HHP, 205
9.11 Applications and conclusions, 205
References, 206
10 Impact of Vacuum packaging, modified and controlled atmosphere on the microbial ecology
of foods, 217
L. Angiolillo, A. Conte, and M.A.D. Nobile
10.1 Introduction, 217
10.2 Vacuum packaging, 218
10.3 Controlled atmosphere, 219
10.4 Modified atmosphere packaging, 220
References, 223
11 Impact of fermentation on the microbial ecology of foods, 226
M. Mataragas, K. Rantsiou, and L. Cocolin
11.1 Introduction, 226
11.2 Fermentations: microbial ecology and activity, 227
11.3 Factors affecting food‐borne pathogen inactivation during fermentation, 227
11.3.1 Factors associated with the product, 228
11.3.2 Factors associated with the microorganisms, 228
11.3.3 Process parameters, 228
11.4 Challenge tests, 229
11.5 Predictive modeling, 230
11.5.1 Behavior of the food‐borne pathogens during inactivation, 230
11.5.2 Kinetic behavior (inactivation) models, 231
11.5.3 Case study: process challenge test for fermented products artificially
contaminated with L. monocytogenes, 233
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 Contents   ix

11.6 Conclusions, 236

References, 236
12 Impact of forming and mixing operations on the microbial ecology of foods: focus
on pathogenic microorganisms, 241
J.C.C.P. Costa, G.D. Posada‐Izquierdo, F. Perez‐Rodriguez, and R.M. Garcia‐Gimeno
12.1 Forming, 241
12.1.1 Description and types, 241
12.1.2 Effect on pathogens/spoilage microorganisms, 242
12.1.3 Predictive models, 242
12.2 Homogenizing, 244
12.2.1 Description and types, 244
12.2.2 Principles of grinding and applications, 244
12.2.3 Effect on pathogens/spoilage microorganisms, 245
12.3 Mixing, 246
12.3.1 Description and types, 246
12.3.2 Principles and applications, 246
12.3.3 Equipment, 247
12.3.4 Effect on pathogens/spoilage microorganisms, 247
References, 248
13 Impact of specific unit operations on food‐borne microorganisms: curing, salting, extrusion,
puffing, encapsulation, absorption, extraction, distillation, and crystallization, 250
E. Ortega‐Rivas, S.B. Perez‐Vega, and I. Salmeron
13.1 Introductory remarks, 250
13.2 Burden of food‐borne illnesses, 250
13.3 Food safety and food quality, 251
13.4 Prevention and control through processing, 251
13.4.1 Introduction: unit operations in food processing, 251
13.4.2 Unit operations for preservation, 252
13.4.3 Unit operations of physical conversions, 257
13.4.4 Unit operations based on separation techniques, 259
13.5 Conclusions and prospects for the future, 260
References, 261
14 Impact of food unit operations on virus loads in foods, 263
D. Li, A.D. Keuckelaere, and M. Uyttendaele
14.1 Introduction, 263
14.2 The use of surrogate viruses to assess inactivation processes, 263
14.3 Virus contamination in food processing, 264
14.3.1 Raw materials, 264
14.3.2 Food handlers, 266
14.3.3 Cross‐contamination during food processing, 266
14.4 Survival of virus in the food processing chain, 267
14.5 Effect of food preservation techniques on the virus load, 267
14.5.1 Reduction of pH, 267
14.5.2 Reduction of aw, 267
14.5.3 Modified atmosphere packaging (MAP), 270
x   Contents

14.5.4 Use of temperature, 270

14.5.5 Washing and decontamination processes, 273
14.5.6 Radiation, 276
14.5.7 High hydrostatic pressure (HHP), 278
14.5.8 Treatment with natural biochemical substances, 279
14.5.9 Hurdle technologies, 280
14.6 Conclusion and perspectives, 280
References, 281
15 Impact of food unit operations on parasites in foods: focus on selected parasites within
the fresh produce industry, 288
L.J. Robertson
15.1 Background and introduction, 288
15.1.1 Fresh produce as a transmission vehicle for parasites, 288
15.1.2 Ranking of food‐borne parasites; occurrence and impacts, 293
15.1.3 Parasite selection for this chapter, 293
15.1.4 Overview of selected parasites, 294
15.2 Detection of selected parasites in fresh produce, 299
15.2.1 Methods used, 300
15.3 Effects of fresh produce treatments on selected parasites, 303
15.3.1 Methods for determining control (particularly removal or inactivation), 303
15.3.2 Effects of different processes, 304
15.4 Conclusion, 315
References, 316
16 Impact of food unit operations on probiotic microorganisms, 327
A. Gandhi and N.P. Shah
16.1 Introduction, 327
16.1.1 Selection criteria for probiotics, 327
16.2 Probiotic products, 328
16.3 probiotics and environmental stress: cellular mechanisms and resistance, 328
16.3.1 Acid tolerance: fermented products, 329
16.3.2 Oxygen tolerance: fermented products, 330
16.3.3 Heat and cold tolerance: dried products, 330
16.3.4 Osmotic tolerance: cheese, probiotic chocolates, 331
16.4 Enhancing stress resistance of probiotics, 332
16.4.1 Microencapsulation, 332
16.5 Conclusion, 334
References, 334

Part III Microbial ecology of food products, 339

17 Microbial ecology of fresh vegetables, 341
J. Zheng, J. Kase, A. De Jesus, S. Sahu, A.E. Hayford, Y. Luo, A.R. Datta,
E.W. Brown, and R. Bell
17.1 Introduction, 341
17.2 Prevalence and diversity of microbial communities on fresh vegetables (post‐harvest), 341
17.3 Post‐harvest persistence, colonization, and survival on fresh vegetables, 342
17.4 Routes of contamination during post‐harvest handling of fresh and fresh‐cut vegetables, 345
 Contents   xi

17.5 Microbial adaptation on produce commodity, 347

17.6 Effective post‐harvest intervention technologies, 348
References, 350
18 Microbial ecology of fruits and fruit‐based products, 358
S. Paramithiotis, E.H. Drosinos, and P.N. Skandamis
18.1 Introduction, 358
18.2 Fresh whole fruits, 359
18.3 Minimally processed fruits, 367
18.4 Processed fruits, 372
18.4.1 Dried fruits, 372
18.4.2 Frozen fruits, 372
18.4.3 Fruit juices, 372
18.4.4 Fermented and acidified fruits, 373
Acknowledgments, 374
References, 374
19 Microbial ecology of cereal and cereal‐based foods, 382
A. Bevilacqua, M. Sinigaglia, and M.R. Corbo
19.1 Introduction, 382
19.2 Sourdough, 382
19.2.1 Description, 382
19.2.2 Microbiota, 383
19.3 Ethnic fermented foods, 384
19.4 Spoilage of cereals and cereal products, 385
19.4.1 Molds on grains, 386
19.4.2 Mold contamination of cereal products, 387
19.4.3 Mycotoxins, 387
19.4.4 Spoilage by yeasts, 387
19.4.5 Rope spoilage, 387
19.4.6 Sour spoilage, 388
References, 388
20 Microbial ecology of nuts, seeds, and sprouts, 390
M.S. Rhee, S.A. Kim, and N.H. Kim
20.1 Introduction, 390
20.2 Definition and classification of nuts, seeds, and sprouts, 390
20.3 Microbial ecology of nuts and seeds, 391
20.3.1 Edible nuts, 391
20.3.2 Potential sources and routes of microbial contamination during manufacturing
of edible nut products, 397
20.3.3 Edible seeds, 399
20.4 Microbial ecology of sprouts and their corresponding seeds, 400
20.4.1 Sprouts sold in market, 400
20.4.2 Seeds used for sprouts production, 406
20.4.3 Changes in microbial ecology during sprout processing and
manufacture, 406
20.5 Implications and perspectives, 409
References, 410
xii   Contents

21 Microbial ecology of eggs: a focus on Salmonella and microbial contamination in post‐harvest

table shell egg production, 416
S.C. Ricke
21.1 Introduction, 416
21.2 Historical and current trends in commercial egg production, 417
21.3 Egg production management on the farm and incidence of Salmonella, 420
21.4 Egg processing and microbial contamination: general aspects, 421
21.5 Microbial contamination during egg collection at the farm to in‐line processing, 423
21.6 Microbial contamination during transportation to off‐line egg processing facilities, 424
21.7 Microbial contamination during egg processing, 425
21.8 Egg washwater and sanitation, 426
21.9 Egg retail and microbial contamination, 428
21.10 Conclusions and future directions, 429
Acknowledgment, 431
References, 431
22 Microbial ecology of beef carcasses and beef products, 442
X. Yang
22.1 Introduction, 442
22.2 Carcass production process, 442
22.2.1 Slaughtering, 443
22.2.2 Carcass dressing process, 443
22.2.3 Carcass decontaminating treatments that are currently used in commercial beef
packing plants, 445
22.2.4 Chilling, 449
22.2.5 Microbiological conditions of carcass sides, 450
22.3 Carcass breaking, 451
22.3.1 Microbiological conditions of beef cuts, 452
22.3.2 Trimmings and offal meats, 455
References, 455
23 Microbial ecology of pork meat and pork products, 463
L. Iacumin and J. Carballo
23.1 Introduction, 463
23.2 Pork meat as a substrate for microbial growth: chemical and physical characteristics, 464
23.2.1 Intrinsic factors, 464
23.2.2 Extrinsic factors, 465
23.3 Microbial ecology of fresh pork meat: sources of contamination and microbial groups, 465
23.4 Microbial ecology of chilled pork meat, 467
23.5 Microbial ecology of vacuum/modified atmosphere packaged pork meat, 468
23.6 Microbial ecology of marinated pork meat, 469
23.7 Microbial ecology of cured and fermented/ripened pork meats, 470
23.8 Microbial ecology of high‐pressure preserved pork meat, 473
References, 474
24 Microbial ecology of poultry and poultry products, 483
S. Buncic, D. Antic, and B. Blagojevic
24.1 Introduction, 483
24.2 Microbial hazard identification and prioritization, 483
 Contents   xiii

24.3 Microbial aspects of poultry processing at abattoirs, 484

24.3.1 Poultry abattoir process steps, 484
24.3.2 Meat safety management in poultry abattoirs, 489
24.3.3 Assessment for process hygiene in poultry abattoirs, 490
24.3.4 Generic framework for comprehensive risk‐based poultry carcass meat safety
assurance for priority hazards, 490
24.4 Microbial aspects of derived poultry meat products, 492
24.4.1 Microbial hazards in poultry meat products, 492
24.4.2 Microbiological criteria applicable to processed poultry meats and products, 494
24.4.3 Principles of microbial safety assurance of poultry meat products, 494
References, 497
25 Microbial ecology of seafoods: a special emphasis on the spoilage microbiota of North Sea
seafood, 499
K. Broekaert, G. Vlaemynck, and M. Heyndrickx
25.1 Introduction, 499
25.2 Total viable counts (TVC s) and microorganisms identified depends on the method
used, 499
25.3 The initial microbiota of marine fish, 501
25.4 Raw seafood, 503
25.4.1 Gutting and filleting, 503
25.4.2 Cooling (icing, superchilling, freezing), 503
25.5 Processing – lightly preserved seafood, 506
25.5.1 Lightly salted, marinated, and cold‐smoked fish, 506
25.5.2 Hot‐smoked fish products, 507
25.5.3 Packaging and storage conditions (temperature), 507
25.5.4 High‐pressure treatment (HPP), 508
25.6 A case study: brown shrimp (Crangon crangon) (adapted from Broekaert et al., 2013), 509
References, 513
26 Microbial ecology of mayonnaise, margarine, and sauces, 519
O. Sagdic, F. Tornuk, S. Karasu, M.Z. Durak, and M. Arici
26.1 Introduction, 519
26.2 Mayonnaise, 519
26.2.1 Microbial ecology of mayonnaise, 520
26.3 Margarine, 523
26.3.1 Microbiological properties of margarine, 523
26.3.2 Microbial spoilage and pathogenic microorganisms, 524
26.4 Sauces and salad dressings, 525
26.4.1 Factors affecting microbial ecology of sauces and dressings, 526
26.4.2 Microbial ecology of sauces and salad dressings, 526
26.5 Conclusion, 527
References, 529
27 Microbial ecology of confectionary products, honey, sugar, and syrups, 533
M. Nascimento and A. Mondal
27.1 Introduction, 533
27.2 Cocoa and chocolate, 533
27.3 Nuts and peanut butter, 535
xiv   Contents

27.4 Honey, 538

27.5 Sugar, 539
27.6 Syrups, 539
27.7 Conclusion, 540
References, 540
28 Microbial ecology of wine, 547
E. Vaudano, A. Costantini, and E. Garcia‐Moruno
28.1 Introduction, 547
28.2 Biodiversity of grape microorganisms, 547
28.3 Microorganism ecology in winemaking, 548
28.3.1 Yeast ecology, 549
28.3.2 LAB ecology, 550
28.4 Microorganism ecology during aging, 550
28.5 Microbial identification by classical methods, 551
28.6 Microbial identification by molecular methods, 551
References, 555
29 Microbial diversity and ecology of bottled water, 560
C.M. Manaia and O.C. Nunes
29.1 Definitions of bottled water, 560
29.2 Characteristics of mineral and spring water, 562
29.3 Useful methods to study bottled water microbiota, 565
29.3.1 Cultivation, 565
29.3.2 Microscopic detection, 567
29.3.3 Total DNA screening, 568
29.4 Microbiological diversity, 568
29.5 Bottling effect, 573
29.6 Microbiological contamination, 574
29.7 A new perspective on microbiological quality and safety, 576
Acknowledgments, 577
References, 577

Part IV Closing section, 581

30 Microbial risk assessment: integrating and quantifying the impacts of food processing
operations on food safety, 583
J.‐C. Augustin, M. Ellouze, and L. Guillier
30.1 Introduction, 583
30.2 Basic processes encountered during food processing operations, 584
30.2.1 Microbial processes, 584
30.2.2 Food‐handling processes, 585
30.2.3 Succession and combination of basic processes, 586
30.3 Risk‐based objectives for each processing operation, 590
30.3.1 Risk‐based metrics, 591
30.3.2 Implementation of process criteria based on food safety metrics with the
ICMSF approach, 592
30.3.3 Implementation of process criteria with quantitative risk assessment models, 594
30.4 Conclusion, 595
References, 596
 Contents   xv

31 Quorum sensing and microbial ecology of foods, 600

V.A. Blana, A. Lianou, and G.‐J.E. Nychas
31.1 Introduction, 600
31.2 Quorum sensing and microbial behavior, 601
31.2.1 Growth, 601
31.2.2 Biofilm formation, 603
31.2.3 Stress resistance, 605
31.3 Quorum sensing and food ecology, 606
31.4 Quorum quenching, 610
References, 611
32 Heterogeneity in Bacillus subtilis spore germination and outgrowth: an area of key
challenges for “omics” in food microbiology, 617
R. Pandey and S. Brul
32.1 Bacterial spores in the food industry, 617
32.2 The Bacillus genus, 618
32.3 Sporulation cycle, 618
32.4 Endospore structure and its resistance, 619
32.5 Spore germination and outgrowth, 620
32.6 Heterogeneity in bacterial (spore) physiology during germination and outgrowth, 623
32.7 Steps towards single‐cell physiology and “omics” measurements, 625
References, 626
33 Role of stress response on microbial ecology of foods and its impact on the fate of food‑borne
microorganisms, 631
A. Alvarez‐Ordóñez, M. López, and M. Prieto
33.1 Introduction, 631
33.2 Acquisition of permanent stress tolerance through adaptive mutagenesis, 631
33.3 Transient adaptive responses to stress: modulation of membrane fluidity as
an example, 634
33.4 Using food components to survive under harsh conditions, 636
33.4.1 Food components and the response to acid stress, 636
33.4.2 Food components and the response to osmotic stress, 638
33.5 The balance between self‐preservation and nutritional competence (SPANC), 639
33.6 Conclusions and future prospects, 641
Acknowledgment, 643
References, 643

Index, 649
List of contributors

A. Alvarez‐Ordóñez V.A. Blana

Teagasc Food Research Centre, Moorepark, Fermoy, Department of Food Science and Human Nutrition,
County Cork, Ireland Laboratory of Microbiology and Biotechnology of Foods,
Department of Food Hygiene and Technology, Agricultural University of Athens, Athens, Greece
University of León, León, Spain
K. Broekaert
L. Angiolillo Institute for Agricultural and Fisheries Research
Department of Agricultural Sciences, Food and (ILVO), Technology and Food Science Unit, Melle,
Environment, University of Foggia, Belgium
Foggia, Italy
E.W. Brown
D. Antic Center for Food Safety and Applied Nutrition, US Food
School of Veterinary Science, Faculty of Health and Drug Administration, College Park, MD, USA
and Life Sciences, University of Liverpool,
Neston, UK S. Brul
Molecular Biology and Microbial Food Safety,
M. Arici Swammerdam Institute for Life Sciences, University of
Food Engineering Department, Yildiz Technical Amsterdam, Amsterdam, The Netherlands
University, Istanbul, Turkey

S. Buncic
J.‐C. Augustin
Department of Veterinary Medicine, Faculty of
Ecole Nationale Vétérinaire d’Alfort, Université
Agriculture, University of Novi Sad, Novi Sad, Serbia
Paris–Est, Paris, France

J. Carballo
P.E.D. Augusto
Área de Tecnología de los Alimentos, Facultad de
Department of Agri‐food Industry, Food and Nutrition,
Ciencias, Universidad de Vigo, Ourense, Spain
Luiz de Queiroz College of Agriculture, University of
São Paulo, Piracicaba, Brazil
E. Carrasco
R. Bell Department of Food Science and Technology,
Center for Food Safety and Applied Nutrition, US Food International Campus of Excellence in the AgriFood
and Drug Administration, College Park, MD, USA Sector, University of Córdoba, Córdoba, Spain

A. Bevilacqua L. Cocolin
Department of the Science of Agriculture, Food and Dipartimento di Scienze Agrarie, Forestali e Alimentari,
Environment, University of Foggia, Università di Torino, Turin, Italy
Foggia, Italy
A. Conte
B. Blagojevic Department of Agricultural Sciences, Food and
Department of Veterinary Medicine, Faculty of Environment, University of Foggia,
Agriculture, University of Novi Sad, Novi Sad, Serbia Foggia, Italy

xvi
 List of contributors   xvii

M.R. Corbo E. Garcia‐Moruno

Department of the Science of Agriculture, Food and Consiglio per la ricerca in agricoltura e l’analisi
Environment, University of Foggia, dell’economia agraria, Centro di Ricerca per l’Enologia
Foggia, Italy (CREA-ENO), Asti, Italy

J.C.C.P. Costa L. Guillier

Department of Food Science and Technology, Laboratory for Food Safety, Université Paris–Est,
International Campus of Excellence in the AgriFood Anses, Paris, France
Sector, University of Córdoba, Córdoba, Spain
A.E. Hayford
A. Costantini Center for Food Safety and Applied Nutrition,
Consiglio per la ricerca in agricoltura e l’analisi US Food and Drug Administration, Laurel, MD, USA
dell’economia agraria, Centro di Ricerca per l’Enologia
(CREA-ENO), Asti, Italy M. Heyndrickx
Institute for Agricultural and Fisheries Research
(ILVO), Technology and Food Science Unit, Melle,
A.R. Datta
Belgium
Center for Food Safety and Applied Nutrition,
US Food and Drug Administration, Laurel, MD, USA
R.A. Holley
Department of Food Science, Faculty of Agriculture
A. De Jesus
and Food Science, University of Manitoba, Winnipeg,
Center for Food Safety and Applied Nutrition, US Food
Manitoba, Canada
and Drug Administration, College Park, MD, USA

L. Huang
P.J. Delaquis
Residue Chemistry and Predictive Microbiology
Pacific Agri‐Food Research Centre, Agriculture and
Research Unit, Agricultural Research Service,
Agri‐Food Canada, Summerland, British Columbia,
United States Department of Agriculture
Canada
Wyndmoor, PA, USA
M.Z. Durak
Food Engineering Department, Yildiz Technical A. Ibarz
University, Istanbul, Turkey Department of Food Technology, School of Agricultural
and Forestry Engineering, University of Lleida, Lleida,
E.H. Drosinos Catalunya, Spain
Laboratory of Food Quality Control and Hygiene,
Department of Food Science and Human Nutrition, L. Iacumin
Agricultural University of Athens, Athens, Greece Dipartimento di Scienze degli Alimenti, Università degli
Study di Udine, Udine, Italy
M. Ellouze
Nestlé Research Center, Nestec Ltd, Lausanne, Switzerland V. Juneja
Residue Chemistry and Predictive Microbiology
A. Gandhi Research Unit, Eastern Regional Research Center,
The University of Hong Kong, Pok Fu Lam, Hong Kong Agricultural Research Service, US Department of
Agriculture, Wyndmoor, PA, USA
R.M. Garcia‐Gimeno
Department of Food Science and Technology, S. Karasu
International Campus of Excellence in the AgriFood Food Engineering Department, Yildiz Technical
Sector, University of Córdoba, Córdoba, Spain University, Istanbul, Turkey
xviii   List of contributors

J. Kase A. Mondal
Center for Food Safety and Applied Nutrition, US Food Center of Food Safety and Security Systems,
and Drug Administration, College Park, MD, USA University of Maryland, College Park, MD, USA

A.D. Keuckelaere S. Mukhopadhyay

Laboratory of Food Microbiology and Food Residue Chemistry and Predictive Microbiology
Preservation, Faculty of Bioscience Engineering, Research Unit, Eastern Regional Research Center,
Ghent University, Ghent, Belgium Agricultural Research Service, US Department of
Agriculture, Wyndmoor, PA, USA
N.H. Kim
Korea University, Seoul, Republic of Korea M.A.D. Nobile
Department of Agricultural Sciences, Food and
S.A. Kim Environment, University of Foggia, Foggia, Italy
Korea University, Seoul, Republic of Korea
M. Nascimento
G. LaPointe Department of Food Technology, Faculty of Food
Department of Food Science, University of Guelph, Engineering, University of Campinas, Brazil
Ontario, Canada
O.C. Nunes
LEPABE – Laboratory for Process Engineering,
D. Li
Environment, Biotechnology and Energy, Faculdade de
Laboratory of Food Microbiology and Food
Engenharia, Universidade do Porto, Porto, Portugal
Preservation, Faculty of Bioscience Engineering,
Ghent University, Ghent, Belgium
G.‐J.E. Nychas
Department of Food Science and Human Nutrition,
A. Lianou Laboratory of Microbiology and Biotechnology of Foods,
Department of Food Science and Human Nutrition, Agricultural University of Athens, Athens, Greece
Laboratory of Microbiology and Biotechnology of Foods,
Agricultural University of Athens, Athens, Greece A.N. Olaimat
Department of Clinical Nutrition and Dietetics,
M. López Hashemite University, Zarqa, Jordan
Department of Food Hygiene and Technology,
University of León, León, Spain E. Ortega‐Rivas
The Postgraduate School, Postgraduate Programme in
Y. Luo Food Science and Technology, Autonomous University
Agricultural Research Service, US Department of of Chihuahua, Chihuahua, Mexico
Agriculture, Beltsville, MD, USA
E.Z. Panagou
C.M. Manaia Laboratory of Food Quality Control and Hygiene,
Universidade Católica Portuguesa, CBQF - Centro de Department of Food Science and Human Nutrition,
Biotecnologia e Química Fina - Laboratório Associado, Agricultural University of Athens, Athens, Greece
Escola Superior de Biotecnologia, Porto, Portugal
R. Pandey
M. Mataragas Molecular Biology and Microbial Food Safety,
Department of Food Science and Technology, Swammerdam Institute for Life Sciences, University of
Laboratory of Food Quality Control and Hygiene, Amsterdam, Amsterdam, The Netherlands
Agriculture University of Athens, Athens, Greece Van Leeuwenhoek Centre for Advanced Microscopy
Visit https://textbookfull.com
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and enjoy exciting offers!
 List of contributors   xix

Section of Molecular Cytology, Swammerdam L.J. Robertson

Institute for Life Sciences, University of Amsterdam, Parasitology Lab, Section for Microbiology,
Amsterdam, The Netherlands Immunology and Parasitology, Department of Food
Department of Food Safety, Safety and Infection Biology, NMBU – Norwegian
Teagasc Food Research Centre, University of Life Sciences, Oslo, Norway
Ashtown, Ireland
D. Roy
S. Paramithiotis Department of Food Science, Faculty of Agriculture and
Laboratory of Food Quality Control and Hygiene, Food Science, Laval University
Department of Food Science and Human Nutrition, Québec, Canada
Agricultural University of Athens, Athens, Greece
O. Sagdic
F. Pérez‐Rodríguez Food Engineering Department, Yildiz Technical
Department of Food Science and Technology, University, Istanbul, Turkey
International Campus of Excellence in the AgriFood
Sector, University of Córdoba, Córdoba, Spain P.N. Skandamis
Laboratory of Food Quality Control and Hygiene,
S.B. Perez‐Vega Department of Food Science and Human Nutrition,
The Postgraduate School, Postgraduate Programme in Agricultural University of Athens, Athens, Greece
Food Science and Technology, Autonomous University
of Chihuahua, Chihuahua, Mexico S. Sahu
Center for Food Safety and Applied Nutrition, US Food
G.D. Posada‐Izquierdo and Drug Administration, Laurel, MD, USA
Department of Food Science and Technology
I. Salmeron
International Campus of Excellence in the AgriFood
The Postgraduate School, Postgraduate Programme in
Sector, University of Córdoba, Córdoba, Spain
Food Science and Technology, Autonomous University
of Chihuahua, Chihuahua, Mexico
M. Prieto
Department of Food Hygiene and Technology,
N.P. Shah
University of León, León, Spain
The University of Hong Kong, Pok Fu Lam Hong Kong

R. Ramaswamy
M. Sinigaglia
Thermal Process Authority, Heinz Innovation
Department of the Science of Agriculture, Food and
and Quality Center, Warrendale, PA, USA
Environment, University of Foggia,
Foggia, Italy
K. Rantsiou
Dipartimento di Scienze Agrarie, Forestali e Alimentari,
Università di Torino, Turin, Italy F. Tornuk
Food Engineering Department, Yildiz Technical
M.S. Rhee University, Istanbul, Turkey
Korea University, Seoul, Republic of Korea
D.O. Ukuku
S.C. Ricke Food Safety Intervention Technologies Research
Center for Food Safety and Department of Food Unit, Eastern Regional Research Center, Agricultural
Science, University of Arkansas, Fayetteville, Research Service, US Department of Agriculture
AR, USA Wyndmoor, PA, USA
xx   List of contributors

S. Unluturk G. Vlaemynck
Department of Food Engineering, Izmir Institute of Institute for Agricultural and Fisheries Research (ILVO),
Technology, Izmir, Turkey Technology and Food Science Unit, Melle, Belgium

M. Uyttendaele E. Xanthakis
Laboratory of Food Microbiology and Food SP-Technical Research Institute of Sweden, Food and
Preservation, Faculty of Bioscience Engineering, Bioscience, Gothenburg, Sweden
Ghent University, Ghent, Belgium
X. Yang
V.P. Valdramidis Agriculture and Agri‐Food Canada Lacombe Research
Department of Food Studies and Environmental Health, Centre, Lacombe, Alberta, Canada
Faculty of Health Sciences, Msida, University of Malta,
Malta J. Zheng
Center for Food Safety and Applied Nutrition, US Food
A. Valero and Drug Administration, College Park, MD, USA
Department of Food Science and Technology,
International Campus of Excellence in the AgriFood
Sector, University of Córdoba, Córdoba, Spain

E. Vaudano
Consiglio per la ricerca in agricoltura e l’analisi
dell’economia agraria, Centro di Ricerca per l’Enologia
(CREA-ENO), Asti, Italy
Part I
Introductory section
Chapter 1

Introduction to the microbial ecology of foods

D. Roy1 and G. LaPointe2
1
Department of Food Science, Faculty of Agriculture and Food Science, Laval University, Québec, Canada
2
Department of Food Science, University of Guelph, Ontario, Canada

1.1 Introduction (diversity and structure), their rate of occurrence,

activities (functionality), and interactions with
Food products become a microbial ecosystem each other (microbial communities) and their
when they are contaminated and colonized environment. Ecological studies also help to
by microorganisms. Fresh foods allow rapid understand the transmission and dissemination
microbial growth due to a high content of nutri­ of pathogens and toxins. Microbial ecology is
ents whereas processed foods correspond to a intimately connected with microbial physiology
harsher environment for growth, reducing the as ecophysiological parameters determine the
natural microbial population associated with activities within individual cells and thus the
raw food. In addition to natural microbiota responses of microbial populations to environ­
related to its origin and environmental condi­ mental influences. These combined effects
tions, food may be contaminated from outside ­control the type of microorganisms capable of
sources during production, processing, storage, growth in a particular food ecosystem (Leistner,
transport, and distribution. Hence, growth and 2000; McMeekin et al., 2010).
activities of microorganisms (bacteria, yeasts, Quantitative microbial ecology relies on pre­
and molds) are some of the major causes of food dictive microbiology to forecast the quantitative
spoilage. However, few microorganisms are evolution of microbial populations over time,
pathogens while many are useful in producing using models that include the mechanisms
desirable changes during food fermentation. ­governing population dynamics and the charac­
A large number of microorganisms can simul­ teristics of food environments. In this respect,
taneously grow in food if the abundance of the diversity of the microbial community of a
nutrients is sufficient. As a consequence, the food ecosystem must be assessed, along with
diversity and occurrence of microorganisms the identification of species and their compara­
present depend on the composition of food, the tive quantification. Traditional microbiological
extent of microbial contamination, and the treat­ techniques (culture‐dependent methods) have
ments applied. Finally, intrinsic and extrinsic been used for decades for this purpose. However,
factors such as temperature, water content, and these methods give a single viewpoint for
oxygen content have a considerable influence describing a portion of the microbial dynamics
on the growth of microorganisms, depending and estimating microbial diversity. Culture‐
on the properties of the microorganisms and on independent techniques based on direct anal­
the interactions among them. ysis of genetic materials (DNA or RNA) are
Microbial ecology of food concerns the increasingly being used for characterization of
study of the type of microorganisms present microbial diversity structure and function. The

Quantitative Microbiology in Food Processing: Modeling the Microbial Ecology, First Edition.
Edited by Anderson de Souza Sant’Ana.
© 2017 John Wiley & Sons, Ltd. Published 2017 by John Wiley & Sons, Ltd.

3
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 “Then we will consider it all settled; it is a banderbust,” and taking
Honor’s arm, she nodded quite an affectionate good night, and
retired into her own quarters.
Precisely at six o’clock the next day the party made a start—the
men on sturdy hill ponies, the ladies in dandies. What can be more
exquisite than a clear April morning on the lower slopes of the
Himalayas? The lake was still and lay half in shadow; the dew
glittered among the cherry blossoms, as if they were set in
diamonds; the low rush-covered marshes were sprinkled with herds
of cattle, and the doves were cooing in the dense woods that
overlooked the misty blue plains. The travellers encountered many
groups of hill folk, going to work among the cultivated patches lower
down, or in the neighbouring tea-gardens, as they passed through a
village, a flock of delightful little brown children sallied out and tossed
freshly plucked monthly roses into the ladies’ laps, “so charmingly
Arcadian and simple,” thought Honor. But she was disillusioned, by
the same little brown elves pursuing them for half a mile, with shrill
demands for “Bucksheesh! bucksheesh!”
As they toiled upwards, the day grew perceptibly warmer, the
ascent steeper. At twelve o’clock they halted by a mountain stream
under some evergreen oaks, and there found an excellent repast
awaiting them. Mrs. Brande’s portly cook had girded up his loins, and
hastened by short cuts and by-paths, and now lay in ambush with
this welcome repast of fowl, cold pie, rolls and coffee; claret and
hock were cooling in a neighbouring stream.
There was some satisfaction in being escort to Mrs. Brande, who
sat on a box, presiding over the table-cloth, and looking the
embodiment of gratified hospitality. When the meal had come to an
end and the men were smoking, she said—
“What’s that in your dandy, Honor? I see you taking as much care
of it as if it was some great treasure; not your new hats, I hope?” in a
tone of real concern.
“No, aunt; it is my violin—a much more important affair.”
 “Nonsense, child! Why did you not leave it with the heavy
baggage?”
“Because it might have been smashed.”
“Well, if it was, it could be mended. We have a very clever Maistry
carpenter at Shirani. I often give him little jobs. My butler—a
Goanese—has a fiddle, too, and of an evening I hear him giving the
other servants a benefit.”
“Perhaps he and I may play duets,” remarked Honor, demurely.
“My dear child!” with a deeply horrified air. “How can you talk in
such a wild way? Captain Waring is shocked—ain’t you, captain?”
“Dreadfully scandalized; and I will only condone the outrage to my
feelings on one condition, that Miss Gordon plays us a solo. Will you,
Miss Gordon? This is the hour and the place.”
Mrs. Brande naturally expected that her niece would require at
least a quarter of an hour’s incessant pressing; and, indeed, in spite
of what the Hodsons had told her, this benighted old person was not
at all sure that it was the correct thing for a woman to play the fiddle.
“Would Mrs. Langrishe allow her girl to do it?” and visions of her own
fat black butler, squatting outside the house in the cool of the day
playing jigs and reels to a circle of enraptured syces and chuprassis,
rose before her mind’s eye!
This vision was quickly dispelled by another. Honor longed for the
sound of her beloved violin, her present audience were not
formidable, and she was not the least nervous. Last time she had
held her fiddle and bow it had been a dull wet afternoon at home—a
type of the worst grey, sullen, English weather. She had played to
them in the drawing-room Schubert’s “Adieu.” Yes, and her mother
had wept. Now, what a different scene, and different listeners! Two
men, almost strangers, prone on the grass, lazily expectant, and, as
far as Captain Waring was concerned, condescendingly ready to be
entertained; a stout lady sitting on a wine-case, with her napkin on
her knee, and her topee quite at the back of her head; a distant
group of scarlet-and-white clad servants; and all around a scene fit
to encircle Orpheus himself. Range after range of purple-blue hills,
rising out of rhododendron and oak forests, a rival across the valley
in the shape of a cuckoo, otherwise a waiting, sympathetic silence.
As the girl took the violin out of its case, Captain Waring could see
that it was in hands that loved it; and noted, moreover, that the said
hands were beautiful—the wrists most daintily modelled. Soon the
bow began to call forth heavenly sounds.
Honor stood up, leaning carelessly against the trunk of a tree, and
seemed wholly unconscious of her audience; her face, which was
turned towards the hills, gradually assumed a rapt exalted
expression, and her playing was in keeping with her attitude and her
eyes. The performance was a revelation—a mixture of great
simplicity, with a distinct note of human passion in its strain. Surely
the music was the voice of this girl’s sweet soul!
The servants boldly came near to hear this new “Miss Sahib” who
drew such marvellous strains from the “sitar.” The very ponies
pricked their ears, a rambling hill cow halted to listen, the competitive
cuckoo was dumb.
The two young men gradually dropped their cigarettes. Mrs.
Brande dropped her jaw. Why, her niece played as well as a man at
a concert! Even better, in her opinion, for this was a tune that
touched her, and that she could understand; those sweet wailing
notes, resembling a human voice, penetrated her opaque
sensibilities, and wafted her to the very gates of Paradise.
Captain Waring surveyed with unaffected curiosity this fair young
musician, with his elbows dug into the grass, his chin resting on his
hands. He knew something about music; the girl played with faultless
taste and absolute purity of tone. He was listening to “linked
sweetness long drawn out” rendered with truly expressive charm.
Here was not the common or ordinary Indian spin, but a modern
Saint Cecilia! He glanced at Mark, to see how this unexpected
transformation had affected him; but Mark’s face was averted, and
he gave no sign, though in reality he was enjoying a debauch of
exquisite musical thoughts.
 Presently the spell, a weird Russian air, died away in a long
sobbing sigh, and, save for a murmur among the servants, there
ensued quite a remarkable pause, broken at length by Mrs. Brande,
who exclaimed as if she had suddenly awoke—
“Very pretty indeed! And how did you like it, Captain Waring?”
“Like it!” he echoed indignantly. “My dear madam, what a feeble
and inadequate expression! Miss Gordon plays magnificently.”
“Oh indeed, no,” she protested. “I can play music that I can feel—
and that is easy, and I began to learn the violin when I was four
years old, so that my fingers are pretty supple; but when I think of
other people’s playing, such as Sarasate, I realize that I am nothing
more than a well-meaning amateur, and never will be otherwise. I
cannot master any excessive technical difficulties. I have no
brilliancy—still,” with a happy little sigh, “I am glad that you liked it.”
“Yes, my dear,” said her aunt, nodding her head approvingly. “And
now let us have something lively. Suppose you play a polka?”
But the violin was already in its case. Honor had laid it there with
the air of a mother consigning an infant to its rest.
“Oh, Miss Gordon, what a shame!” expostulated Mark Jervis. “I
could lie on this sunny slope, under the rhododendrons, listening to
you for days.”
“You would not find it very comfortable in the rains,” remarked Mrs.
Brande, with some asperity. She did not approve of penniless young
men thus launching compliments at her accomplished niece. “And
now we had better be getting on, if we are to reach Binsa before
dark.”
The next and last day of their march the party were proceeding as
usual in pairs; Honor and Captain Waring led the van, whilst Jervis
and Mrs. Brande, who was a heavy load, lagged behind. The further
they journeyed, the steeper grew the precipices, the wilder the
scenery, the narrower the paths. At one place in the woods, high
above them, grazed a herd of so-called tame buffaloes—tame with
natives, wild with Europeans. The huge bull, with his hairy head and
enormous horns—though he carried a bell—was tame with no one!
Hearing strange voices below, he lifted up his hideous china-blue
eyes, stared fiercely about him, and then came crashing downhill for
some dozen yards, but his prey—Honor and her escort—had already
passed by, and were out of reach. He stood still in a meditative
attitude, and gave vent to an angry and disappointed bellow.
After a considerable interval, another group came into view. Mrs.
Brande’s gay jampannis and scarlet dandy rug settled the question.
In half a moment he had blundered through the undergrowth, and
placed himself in a warlike attitude upon the path—exactly six yards
ahead of the party. The unanimity with which Mrs. Brande’s bearers
dropped her, and fled up trees, was only equalled by the agility
displayed by the lady herself, in leaping out of the dandy and
scrambling down the khud! Nothing remained on the track but the
empty vehicle, the buffalo, and Jervis.
He promptly jumped off his pony, snatched up a jampanni’s pole,
on the end of which he raised the red rug, and boldly advanced like a
matador in the arena. When the bull lowered his ponderous head to
charge, he threw the rug over his horns with as much coolness and
dexterity as if he had merely to deal with a stuffed animal! But this
animal was dangerously animated. Rushing furiously forward, he
tumbled blindly over the dandy, and with a loud crash, rolled down
the khud, which, luckily for him (and Mrs. Brande) was not of sheer
descent. The lady’s piercing screams attracted the notice of her
niece, and—of what was far more to the purpose—the boy who was
in charge of the herd. Probably he had been fast asleep, but he now
came racing through the brushwood, routed up the buffalo, whose
fall had undoubtedly quenched his spirit, and drove him away, laden
with the hearty curses of the jampannis. These valiant gentlemen
had now descended to mother earth, as brave as lions. The rug was
in ribbons, the dandy in matchwood, but no one was injured. “What
was to be done?” inquired Captain Waring, vainly struggling to
preserve a grave countenance, as he saw Mrs. Brande, who
presented a truly distressing spectacle, emerging from the bushes,
on her hands and knees. The back of her dress was split right across
the shoulders, her veil hung round her neck, and she was covered
with sand and bits of twigs.
 Mark had hastened to her assistance, and her niece, as she
picked up her topee and umbrella, asked anxiously “if she was hurt?”
“No,” she panted, sitting down and dusting herself with her
handkerchief, “I’m not a bit the worse.”
“But your dandy is in smithereens!” said Captain Waring. “What is
to be done?”
“I know what has been done. Young man,” solemnly addressing
herself to Jervis, “you saved my life, as sure as I sit here, and you
stand there. If you had not had the courage to throw the rug over his
head, he would have come down the khud, and gored me to death—
I’m not a woman of many words” (fond delusion) “but I won’t forget it
—nor will P.” In moments of unusual excitement, or when with her
intimates, she invariably spoke of her husband as “P.”
“Oh, Mrs. Brande,” he replied, “you think a great deal too much of
it—it was only a buffalo.”
“Only a buffalo!” she repeated. “You little know them; in another
minute I’d have been only a corpse. They are the most dangerous
brutes you can come across, and so cunning. Ha,” changing her
voice to another and sharper key, “Jait Sing, you base coward! I shall
cut every one’s pay two rupees. I’ve a mind to stop your wood
tickets. What a contrast to you,” she pointed her fat finger straight at
Jervis. “Lions, indeed, as all these Sings call themselves—pretty
lions—you are the bravest young man I ever saw!”
“Oh come, I say, Mrs. Brande,” expostulated Waring, playfully.
“You don’t know what I could do if I tried.”
“Well, as you did not try, I cannot say,” she answered dryly.
“It’s not such a marvellous feat, driving off an old buffalo——”
“Depends upon the humour the buffalo is in; and I’m surprised at
you belittling your own cousin, instead of being proud of him,”
pursued the lady with considerable heat, and entirely forgetting her
intended rôle with respect to this millionaire.
“How are you to get on, aunt?” inquired Honor; “but of course you
must go in my dandy and I can walk.”
 “By no means, Miss Gordon; you shall ride my pony,” said Captain
Waring. “He has a grand roomy old saddle and a fine broad back,
and I will hold you from slipping off.”
To this arrangement Mrs. Brande (who had now recovered her
composure and her wits) saw no objection. Quite the contrary, it was
a capital idea. As for herself, she felt so shattered and so nervous,
that she could not allow Mr. Jervis out of her sight.
They were now within seven miles of Shirani, and oh! what
interminable miles—they seemed leagues—leagues of dreary
monotonous road, winding and twisting round barren fawn-coloured
hills, and apparently taking them straight into the very heart of Asia.
They wound up and down valleys, to the crest of a range, which hid,
as they fondly hoped, long-looked-for Shirani. Alas! it but gave them
a view of yet another valley—yet another rounded hill slope. Honor
was not surprised to hear that a lady of her aunt’s acquaintance, on
her first visit, had, after a series of these maddening
disappointments, collapsed on the journey, and given way to a storm
of hysterical tears. Sometimes Honor walked—walked by
preference, but at others, she mounted the pony in deference to her
chaperon’s wishes. She did not enjoy her ride, it consisted of a
gradual slide, slide, slide, a recover, then slide, slide, again. She
declined Captain Waring’s eagerly tendered arm—support was twice
as irksome as walking. Would this detestable road never, never,
come to an end?
Ah, there were the pine trees of Shirani at last! In another twenty
minutes, they were among them. As the little party debouched into
the mall, Mrs. Brande heading the procession, Honor bringing up the
rear, with Captain Waring leading her pony, they came face to face
with Mrs. Langrishe, walking with her most stately air, between a
soldierly looking man and a small, beautifully dressed, fair-haired
girl.
Yes, she could not have failed to notice and take in the full
significance of Mrs. Brande’s rentrée (indeed she and her rival had
exchanged bows), and dusty, hot, and thirsty, as that lady was, this
was one of the happiest and proudest moments of her life!
 CHAPTER XVI.
A MESSAGE FROM MISS PASKE.

Although she had only caught a fleeting vision of Mrs. Brande’s

niece, Mrs. Langrishe had sharp eyes, and one glance had been
sufficient to assure her that the girl was not the least like what she
had expected. She was slim and dark, and, though covered with
dust, and wearing a frightful one rupee topee, undeniably a lady, and
not at all of the dairymaid type.
And how exultant the old woman had looked! Literally puffed out
with pride, as she was carried past, with the millionaire in close
attendance. Not that that detail was of the slightest consequence.
Lalla knew him intimately, and she would get her to write him a nice,
friendly little note, and ask him to drop in to tea.
Meanwhile Honor had been presented to her uncle, who, far from
being disappointed, was agreeably surprised to find that she was the
image of his favourite sister Hester, who had died when she was
eighteen. This resemblance (which he kept to himself) ensured the
new arrival an immediate entrée to her uncle’s good graces. And
Mrs. Brande, accustomed to his cool and rather cynical manner, was
amazed at the warmth of the reception he accorded to his hitherto
unknown niece.
For several days the young lady was kept at home in strict
seclusion, until her complexion had recovered the journey and her
boxes had arrived from the railway. Her aunt was determined not to
submit her treasure to the fierce gaze which beats upon a newly
arrived girl, until she was altogether at her best. She, however, could
not close her doors to numerous ladies who came to call upon Miss
Gordon, and thus secure an early and private view. Honor was
compelled to sit in state in a hideous drawing-room, where every
colour was shouting at another, and listen to her aunt telling visitors
how beautifully she played the fiddle, and what long hair she had,
and how she took threes in shoes, and how useful she was in the
house already. Also, she did not spare them full particulars of the
buffalo adventure, nor fail to sing loud praises of Mr. Jervis, or to
enlarge on his cousin’s agreeable escort and particular attentions en
route. Then Mrs. Brande discussed her servants and the outrageous
price of ghee and charcoal.
“Come, let us sit in the verandah,” whispered Mrs. Sladen, who
had read the girl’s expressive face. “You will get quite used to it,” she
continued, when they were outside; “you will do it yourself some day.
We all do; but you will have a very happy home here, in spite of the
price of potatoes! Your aunt is delighted with you, as you may see,
and you will soon have plenty of topics to discuss. She has been
lonely enough till now. She and Mr. Brande, although much attached
to one another, have few tastes in common. He is fond of literature,
and devoted to tennis and rackets; and although he is older, he is so
active that he seems years her junior. Your coming has given her a
fresh start and new pleasures. She is a dear, good woman, and as
single-hearted as a little child.”
Mrs. Sladen and Honor had taken to one another at once. Honor
had been down (after dusk) to Mrs. Sladen’s house—been
presented to Colonel Sladen, and shown the photographs of Mrs.
Sladen’s little girls—Charlotte and Mabel, and had heard their last
letters—a proof that she was in high favour with their mother. Honor
was not accustomed to sitting with her hands before her, and
promptly found occupation in various ways—she ran messages,
wrote notes and orders, arranged flowers, and ventured on
respectful suggestions with regard to the drawing-room, a fine
apartment, expensively furnished in the worst taste imaginable—a
supreme contrast to Mrs. Langrishe’s room, which was the prettiest
in Shirani. People little suspected how that leisurely lady dusted it
entirely herself, shook out draperies, arranged flowers, and washed
the china ornaments with her own delicate hands. Her room, as she
understood it, made an effective background for herself—and she
spared no pains to frame Ida Langrishe in the most becoming
fashion. The floor was covered with fine old prayer-rugs, the tables
were strewn with curios, the walls hung with valuable water colours,
and scattered at suitable intervals were inviting armchairs.
Ill-natured people assured one another that the Persian rugs,
carvings, and silver bowls were all so many offerings from “men.”
Even so Mrs. Langrishe would have been the first to admit,
“Presents to Granby and myself. Colonel Greene, a dear old thing,
brought us the carpet from Peshawar; and Mr. Goldhoofe sent those
silver things from Delhi. I must say that our friends never forget us.”
Mrs. Langrishe, as we know, had fully determined to hand over the
drawing-room to her niece, it would be such good practice for the
child, and really the flowers took up an hour every morning. She
would find many ways of making Lalla useful. But that young lady
steadily objected to these plans, she immediately made her aunt
aware that she considered herself merely ornamental. “Oh dear no!
she never arranged flowers, she had no taste in that line, and
besides, it would spoil her hands. Dust the drawing-room! dear Aunt
Ida must be joking; why, that was the bearer’s business. Get out the
dessert! oh!” with a peal of ringing laughter, “she was not to be
trusted. She would eat every chocolate, and all the best French
sweets!”
So whilst Mrs. Langrishe laboured, as usual, over her household
tasks, her fair niece, with a locked door, lay upon her bed, reading a
novel, tried new experiments in the hairdressing line, or wrote notes.
No, no; she had not come to Shirani to be a lady-help. She had
always heard that her aunt Ida was very clever; but, luckily, she had
her wits about her also!
During Honor Gordon’s period of enforced retirement, she went
early every morning for a solitary walk along a pretty sandy road,
that wound among the dark aromatic pine woods—a road with sharp
angles, and deep leafy ravines, green with ferns and ivy. It was early
in May, and the ground was strewn with pine-needles, which
deadened the footfall; the firs were thin and bare, and through their
dark branches she caught glimpses of the snows, that like a great
white rampart hung in mid-air, between a brilliant blue sky and an
opal-tinted mist. Honor enjoyed these rambles immensely, though
she rarely met a soul, save a syce exercising a horse, or an ayah
wheeling a perambulator. Her sole companion was “Ben,” who luckily
had “taken to her,” and with whom she had established relations of
such a friendly character, that she had actually been installed in the
unexpected position of his “aunt.”
Occasionally they made joint excursions down the khud, he in
search of the private larders of other dogs, she in quest of ferns and
moss for table decoration. Ben was a personage of such importance
at Rookwood that he demands half a chapter to himself. He was a
dog with fixed opinions, and hated Mrs. Langrishe—and one or two
other people—in the same degree that he hated cold boiled meat.
Sport was his passion, the chewing up of Suède gloves his
weakness. He was a fox-terrier with a history. As a pup, he had been
presented by a man to a girl, on the principle of “love me love my
dog,” but alas, the false maiden had loved neither the one nor the
other; she heartlessly jilted the man, and abandoned the dog to his
fate. However, her ayah (prudent soul) ere she went down the hill,
sold the pup to a bheestie for the sum of two annas (an ancient
debt), he happened to be Mrs. Brande’s servant, and was
excessively vain of his purchase, but left him most of the day tied by
a strip of pink calico to a conspicuous tree in her compound, where
he suffered him to “eat the air,” and but little else. Mrs. Brande, en
route to feed her well-to-do fowls, noticed the famishing animal; and
as she often threw him a crust, he naturally hailed her advent with
extravagant demonstrations of delight and feeble yelps of joy. Her
easily softened heart was touched by the raptures of the starving
puppy, and after some parley she bought him from the bheestie for
the sum he swore he had paid—to wit, ten rupees—in order to feed
him up and get him a good master. But Ben was thoroughly satisfied
with his present quarters, and soon made himself completely at
home. He displayed an easy intimacy with armchairs and cushions,
he had undoubtedly been accustomed to sweet biscuits and to good
society, and his mistress pointed out with just pride that he
understood English perfectly! Of course she eventually adopted
“Ben,” he made himself indispensable, he refused to be separated
from his patroness, and became her shadow, and soon ceased to be
a shadow himself. He grew from a dirty, starving, shivering whelp,
into an extremely handsome dog, with a fine gloss on his coat. Did
he ever remember his own evil days, as he lounged of an afternoon
sunning himself at the gate of Rookwood, and passed in scornful
review, curs less happy and of low degree? Are dogs snobs?
Whether snob or not, Ben was brave, he lowered his tail to none,
and when the big wild cat that created such havoc among the
poultry, went to ground under the messhouse, “Ben Brande,” as he
was called, was the only one of the assembled mob of terriers, who,
as a looker on expressed it, “was man enough to follow him, kill him,
and drag him out.” Ben Brande lost an eye thereby, but gained a
magnificent reputation.
Of course Ben was spoiled. His mistress talked to him incessantly;
he had his own little charpoy in her room, his morning tea in her
company, and now and then he was permitted to invite his pal
“Jacko,” a red terrier, to dine and spend the day! (Once they had
elected to spend it quietly in Mr. Brande’s dressing-room, where they
devoured several pairs of boots, a sponge-bag, and the back of
“Nancy.”) Ben escorted his mistress in her walks and drives. Many a
time she went out solely on his account, and it was an indisputable
fact that he had favourite roads, and his “grandmamma”—as the
infatuated lady called herself—always studied his wishes. On those
occasions when “his grandpapa and grandmamma” were dining
abroad, he never went to bed, but established himself at the
entrance until their return (however late), and passers-by could
always tell that the Brandes were at a “burra khana” when they saw
an upright little white figure sitting by the gatepost. Indeed it was
whispered, that the reason Mrs. Brande was always so early to
depart, was simply that she did not like to keep Ben waiting up! She
never said so, but every one knew that Ben was the real motive for
her premature departure. And this was the animal who now
accompanied Honor, and who had accorded her his patronage and
friendship. One morning, as they were strolling homewards, he with
a large stone in his mouth, and she carrying an armful of ferns, they
nearly came into collision with another couple—the angles were
abrupt—walking noiselessly on pine needles. They proved to be
Toby Joy, who was also attended by a dog, and sauntering along
hand-in-hand with a young lady, a dainty, white-skinned little person,
with fluffy light hair, small keen eyes, admirably arched brows and a
tip-tilted nose.
Honor was by far the most embarrassed of the trio, and blushed a
good healthy blush—of which she was heartily ashamed. Why
should not other people enjoy the delicious morning air? As to
walking hand-in-hand, she ought to be the last person to object; had
she not walked hand-in-hand herself with an absolute stranger?
“Good morning, Miss Gordon,” said Toby, slowly relinquishing Miss
Paske’s fingers, and doffing his cap. “So you have got up here all
right in spite of the buffalo! Let me introduce you to Miss Paske.”
The girls bowed, and looked at one another gravely.
“We are getting up that burlesque I told you about, and have come
out early to study our part together.”
“How praiseworthy of you,” said Honor, in simple good faith. “And
what is the piece to be?”
“The Babes in the Wood,” responded Miss Paske with an odd
smile, and looking Honor over with her bright little eyes. “Don’t you
think it will be suitable to the dear simple people at Shirani?”
“I really don’t know,” replied the other, with a puzzled face.
“Well, I hope you will come to see it,” and with a patronizing nod
she moved on. But Ben and Jumbo (Mrs. Langrishe’s dog) were not
disposed to part thus! The household feud had evidently extended to
them. They had been tiptoeing round one another for some time,
with considerable stiffness in their gait, emitting low and insulting
growls, that now culminated in a sort of gurgling snarl, as they flew at
one another’s throats. Miss Paske gave a little stifled shriek, and
scrambled hastily up the bank, whilst Honor and Toby made
desperate attempts to separate the combatants. They each caught
hold of a dog by whatever came first, leg or tail; but the dogs refused
to be parted, and to and fro, and up and down, they struggled and
scrambled in a mutual frenzy. Meanwhile, Lalla, who was now at a
safe elevation, actually appeared delighted at the performance, and
laughed and clapped her hands ecstatically. At last, by the expedient
of pouring sand on their heads, the dogs were choked off, and each
side was bottle-holder to a furious, panting, struggling animal.
“I think we had better separate at once,” gasped Honor, who only
restrained Ben with the greatest difficulty.
“Yes, the sooner the better,” agreed Toby, who was also wrestling
with an eager armful.
As Honor turned homewards, with Ben hanging longingly over her
shoulder, Miss Paske, who had tripped down from her coign of
’vantage, called after her, in her sweetest, clearest tones—
“Be sure you tell Mrs. Brande, that her dog got the worst of it.”

END OF VOL. I.

PRINTED BY WILLIAM CLOWES AND SONS, LIMITED, LONDON

AND BECCLES.
 Transcriber’s Notes
Punctuation errors/omissions have been fixed.
Page 21: “you have jus” changed to “you have just”
Page 246: “Grandby and myself” changed to “Granby and myself”
*** END OF THE PROJECT GUTENBERG EBOOK MR. JERVIS,
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