Development of a microbial model for the combined effect of temperature and pH on spoilage of ground meat, and validation of the model under dynamic temperature conditions

Abstract

The changes in microbial flora and sensory characteristics of fresh ground meat (beef and pork) with pH values ranging from 5.34 to 6.13 were monitored at different isothermal storage temperatures (0 to 20 degrees C) under aerobic conditions. At all conditions tested, pseudomonads were the predominant bacteria, followed by Brochothrix thermosphacta, while the other members of the microbial association (e.g., lactic acid bacteria and Enterobacteriaceae) remained at lower levels. The results from microbiological and sensory analysis showed that changes in pseudomonad populations followed closely sensory changes during storage and could be used as a good index for spoilage of aerobically stored ground meat. The kinetic parameters (maximum specific growth rate [mu(max)] and the duration of lag phase [lambda]) of the spoilage bacteria were modeled by using a modified Arrhenius equation for the combined effect of temperature and pH. Meat pH affected growth of all spoilage bacteria except that of lactic acid bacteria. The "adaptation work," characterized by the product of mu(max) and lambda(mu(max) x lambda) was found to be unaffected by temperature for all tested bacteria but was affected by pH for pseudomonads and B. thermosphacta. For the latter bacteria, a negative linear correlation between ln(mu(max) x lambda) and meat pH was observed. The developed models were further validated under dynamic temperature conditions using different fluctuating temperatures. Graphical comparison between predicted and observed growth and the examination of the relative errors of predictions showed that the model predicted satisfactorily growth under dynamic conditions. Predicted shelf life based on pseudomonads growth was slightly shorter than shelf life observed by sensory analysis with a mean difference of 13.1%. The present study provides a "ready-to-use," well-validated model for predicting spoilage of aerobically stored ground meat. The use of the model by the meat industry can lead to effective management systems for the optimization of meat quality.

FIG. 1.

Representative growth curves of the spoilage microflora on ground meat: ground beef with pH 5.34 (a and b) and ground pork with pH 6.13) (c and d) stored aerobically at 0°C (a and c) or 10°C (b and d). Media: PCA, plate count agar (total aerobic populations); CFC, cetrimide fusidin cephaloridine (pseudomonads); STAA, streptomycin-thallous acetate-actidione agar (Brochothrix thermosphacta); MRS, Man Rogosa Sharp (lactic acid bacteria); VRBG, violet red bile glucose agar (Enterobacteriaceae).

FIG. 2.

Square root of sensory score values of ground pork with pH 6.13 during aerobic storage at 0, 5, 10, and 15°C.

FIG. 3.

Experimental conditions tested to generate the models. Area enclosed by the ground of ABCDEF illustrates the interpolation region of the model.

FIG. 4.

Predictions of the modified Arrhenius model (equation 1) for the effect of temperature and pH on the maximum specific growth rate (μ_max) of the different spoilage bacteria (a, pseudomonads; b, Brochothrix thermosphacta; c, lactic acid bacteria; d, Enterobacteriaceae) on ground meat. Lines represent predictions of equation 1 at three different initial pH values of meat. Points represent observed values of μ_max.

FIG. 5.

Effect of initial pH of meat on the natural logarithm of the μ_max × λ product of the different spoilage bacteria (a, pseudomonads; b, Brochothrix thermosphacta; c, lactic acid bacteria; d, Enterobacteriaceae). Points represent observed values. Solid lines show the linear regression line. In panels a and b, dotted lines show the prediction of equation 3.

FIG. 6.

Comparison between observed (points) and predicted (lines) growth of spoilage bacteria (a, pseudomonads; b, Brochothrix thermosphacta; c, lactic acid bacteria; d, Enterobacteriaceae) on ground pork (pH 5.65) stored at periodically changing temperature (24 h at 0°C and 24 h at 10°C).

FIG. 7.

Comparison between observed (points) and predicted (lines) growth of spoilage bacteria (a, pseudomonads; b, Brochothrix thermosphacta; c, lactic acid bacteria; d, Enterobacteriaceae) on ground pork (pH 5.95) stored at periodically changing temperature (12 h at 0°C, 6 h at 10°C, and 6 h at 15°C).

FIG. 8.

Comparison between observed (points) and predicted (lines) growth of spoilage bacteria (a, pseudomonads; b, Brochothrix thermosphacta; c, lactic acid bacteria; d, Enterobacteriaceae) on ground pork (pH 6.10) stored at periodically changing temperature (6 h at 2°C, 6 h at 10°C, and 6 h at 20°C).

FIG. 9.

Comparison between observed (points) and predicted (lines) growth of spoilage bacteria (a, pseudomonads; b, Brochothrix thermosphacta; c, lactic acid bacteria; d, Enterobacteriaceae) on ground pork (pH 6.10) stored at periodically changing temperature (18 h at 5°C and 6 h at 20°C).

FIG. 10.

%RE values for the comparison between observed and predicted growth of spoilage bacteria (a, pseudomonads; b, Brochothrix thermosphacta; c, lactic acid bacteria; d, Enterobacteriaceae) on ground pork (pH 6.10) stored at changing temperature.