The Microbiology of Dirty Eggs Treated in Various Ways and Stored at Different Temperatures and Humidities1

MICROBIOLOGY OF DIRTY EGGS Schultze, A. B., and C. W. Turner, 1945. The determination of the rate of thyroxine secretion by certain domestic animals. Missouri Agr. Exp. Sta. Res. Bui. No. 392. Shaffner, C. S., 1948. The influence of thyroproteinfeeding on semen quality. Poultry Sci. 27: 527528. Shaffner, C. S., and F. N. Andrews, 1948. The influence of thiouracil on semen quality in the fowl. Poultry Sci. 27: 91-102.

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Titus, H. W., and W. H. Burrows, 1940. Influence of wheat germ oil on semen production of cockerels. Poultry Sci. 19: 295-298. Wheeler, R. S., E. Hoffmann and C. L. Graham, 1948. The value of thyroprotein in starting, growing and laying rations. I. Poultry Sci. 27:103-111. Wheeler, R. S., and E. Hoffmann, 1948. The value of thyroprotein in starting, growing and laying rations. II. Poultry Sci. 27: 509-514.

W. A. M I L L E R

Department of Bacteriology, Kansas Agricultural Experiment Station, Manhattan, Kansas (Received for publication October 22, 1953)

T

HE problem of the commercial disposition of dirty eggs is one of considerable importance to the poultry industry. Numerous recommendations or suggestions have been proposed by individuals and organizations for handling dirty eggs with the hope that microbial penetration and subsequent spoilage might be reduced or prevented. Among these practices or recommendations have been included washing with water or water containing a detergent, followed by treatment with such chemical agents as sodium hydroxide, acids, "Roccal" (a quaternary ammonium compound); buffing; pasteurization; etc. One of the objectives in this investigation has been to compare and evaluate some of the suggested methods and materials used in handling and treating dirty eggs. Physical and organoleptic evidences of deterioration and spoilage have been 1 Contribution No. 289. Department of Bacteriology, Kansas Agricultural Experiment Station, Manhattan, Kansas.

widely used in ascertaining changes in eggs due to growth of microorganisms. Such criteria are inadequate for detecting early phases of microbial growth in experimental work, consequently quantitative and qualitative bacteriologic analyses were made on each individual egg throughout this investigation. Funk (1948) presented data based on experiments with dirty eggs in the spring of 1940, which indicated that when the temperature of the wash water was lower than the internal temperature of the egg, losses in storage were definitely greater compared with storage losses in eggs washed in water the temperature of which was higher than the internal egg temperature. On the contrary, in a similar group of experiments conducted in the spring of 1941, storage losses among washed dirty eggs were not influenced by the temperature of the wash water; all lots kept well. Treating the surface of shell eggs with certain chemical agents did not effectively prevent spoilage in storage. Starr et al. (1952) found no consistent

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The Microbiology of Dirty Eggs Treated in Various Ways and Stored at Different Temperatures and Humidities 1

736

W. A. MILLER

Forsythe et al. (1953) investigated the microbiological populations on and in shell eggs, and suggested that plate counts on individual eggs were of greater value than candling, in obtaining data on the penetration and growth of microorganisms in shell eggs.

PROCEDURE

In the microbiological analyses of eggs in this study essentially the same techniques and materials were employed as previously described by Miller and Crawford (1953). The eggs were obtained from the Perry Packing Company, Manhattan, Kansas, and the Poultry Department, Kansas State College, Manhattan. Washing was performed by scrubbing the eggs lightly with a small hand brush. Thirty-six eggs were immersed in clean tap water containing a detergent (1 percent solution), scrubbed, and rinsed directly under the tap, an operation requiring about 15 minutes. Temperature of the water was approximately 68 to 70° F. The internal temperature of the eggs was not above 70°F. when washing commenced, but when a large number of eggs were handled the temperature of some of them may have exceeded the water temperature toward the end of the washing process, especially on a hot day. However, no apparent discrepancies in results were observed due to this warming of some of the eggs. Batches of eggs were removed from cold storage at monthly intervals and kept at 50 to 60°F. during the one to three weeks interval during which bacteriological analysis was conducted. Plate counts per ml. on some off odor eggs were in the hundreds of millions or even more than 1 billion; however, all such counts are recorded in this paper as more than 10 million per ml. A. Groups 1 and 2 Eggs (Table 1) The dirty eggs in group 1 were obtained from the Kansas State College poultry farm, in March 1949, by allowing the chickens to run in muddy lots. During collection, the eggs were held in an egg cellar at 41°F. to 46°F. for a maximum of 7 days before processing and storing. The eggs were stored at a temperature of 59°F.

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difference in grade between washed and unwashed eggs when conventional candling alone was used in measuring quality. However, the use of ultraviolet light enabled candlers to identify inedible eggs by their flourescence (especially washed eggs). Lorenz and Starr (1952) cited Johns and Berard (1946) who observed that soil organisms were more instrumental in producing spoilage than intestinal organisms, since additional spoilage was obtained by applying mud to shells previously soiled with feces; they indicated that the importance of soil in causing increased egg spoilage may explain certain discrepancies in previously reported data. Lorenz et al. (1952) studied the effect of washing eggs on 22 ranches; 21 of these producers washed all their eggs (clean as well as dirty). Spoilage was determined by candling and testing with ultraviolet light after 6 months in commercial cold storage. Spoilage of eggs from the various ranches varied from 0 to 38 percent. No relationship was observed between the amount of spoilage and the degree of cleanliness before washing. The authors stated that there was no apparent relationship between spoilage and any factor suggested by previous studies. During this survey it was found that 97 percent of 606 spoiled eggs were fluorescent under ultraviolet light when broken out, presumably due to the growth of organisms belonging to the genus Pseudomonas. One-fourth of these fluorescent eggs were not abnormal either in odor or appearance.

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MICROBIOLOGY OF DIRTY EGGS TABLE 1.—Microbial content of eggs stored up to eight months at 60° to 65''F. and a relative humidity of 60 to 65 percent. Storage room extremely dirty

Percent of eggs containing significant numbers of

Group 1. Dirty (collected Mar. 1949, Kans. State College Poultry Farm) No. of Eggs

Spoilage bacteria*

Treatment Scrubbed in a detergent

Rinsed in water

Scrubbed in a detergent Scrubbed in water

Rinsed in water Rinsed in water

100 100

Scrubbed in water S o a k e d i n l % N a O H , 20 min. Scrubbedin water

100

Hand buffed (sandpaper) some dirt remained

100

Scrubbed in water

"Roccal" (1. Oz. Air dried to 4 gal.) 2 % lactic acid Air dried Pasteurized in wa- Air dried ter (167°F. 20 sees.) Air dried Rinsed in 1% Air dried NaOH

Oiled

4

5

Oiled Oiled

18 1

10 1

Oiled Oiled

9 7

10 10

Oiled

3

5

Group 2, Dirty (collected Sept., 1949, Kans. State College Poultry Farm)

100 100 100 100 100

Thermostabilized in water at 131°F. for 20 minutes Scrubbed in water Soaked in 1% N a O H Scrubbed in water Rinsed in 1% 20 minutes NaOH Scrubbed in water Hand buffed (sandpaper) some dirt remained Dirty (not washed)

Air dried

Oiled

8

Air dried Air dried

Oiled Oiled

25 21

12 (cocci) 12 (molds) 7 12

Air dried

N o t oiled Oiled N o t oiled

18 14 13

5 14 6

* A majority of these eggs contained millions of Gram negative spoilage bacteria per ml. t Counts not recorded unless greater than 1,000 per ml. (10 colonies on a plate containing .01 ml. of whole e

to 64°F. and a relative humidity of 60 to 65 percent and were exposed to contamination by chickens, litter, and mice throughout storage. Samples were examined periodically during the following 8 months, and the number of eggs found to contain significant numbers of bacteria (Pseudomonas, coliforms, cocci, etc.) varied from 1 to 18 per cent.

The percentage of eggs containing cocci paralleled rather closely the percentage of eggs yielding Gram negative rod types (hereinafter referred to as "spoilage" bacteria). Isolated strains of cocci did not grow below 41°F. Mold spoilage was negligible. Group 2 consisted of dirty eggs collected at the College poultry farm during

TABLE 2.—Microbial content of eggs stored up to nine months in commercial cold storage at approximately 32°F. and 90 to 95 percent relative humidity Percent of eggs containing significant numbers of

Group 3. Dirty current receipts (Oct., 1951, from a local packing plant) No. of Eggs

Spoilage bacteria

Treatment Scrubbed in a detergent Scrubbed in a detergent Scrubbed in a detergent

Rinsed in water Rinsed in water Rinsed in water

200 200

Scrubbed in a detergent Scrubbed in a detergent

Rinsed in water Rinsed in water

200

Hand buffed (sandpaper). Some dirt remained

Rinsed in 1% N a O H "Roccal" 1% Sodium bisulfite, plus cone. HC1 to liberate sulfur dioxide Thermostabilized in water (131°F. for 20 min.)

Cocci

Air dried Air dried Air dried

Oiled Oiled Oiled

7 4.5 5

Air dried Air dried

Oiled Oiled

1 1

Oiled

2

1

Oiled

1.2 (2 eggs)

0.6 (1 egg)

None found

2.2 (4 eggs)

Total 1.7 Percent

200 200 200

1 1 2

0.5 2

Group 4. Clean current receipts (Oct., 1951, from a local packing plant). 168

Not washed

180

N o t washed

Group 5. Clean 1 to 2 days old. (collected Oct., 1951, Kans. State College Poultry F a r m ) . Oiled

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100 100 100

Cocci t

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W. A. MILLER

B. Groups 3, 4 and 5 (Table 2) Group 3 consisted of 1,200 dirty, current receipt eggs purchased from a local packing plant in October 1951. The eggs were divided into 6 lots of 200 eggs each, treated differently and stored commercially at 32°F. Periodic analyses extending over a nine-month period disclosed that the number of eggs containing significant numbers of spoilage bacteria in the variously treated lots ranged from 1 to 7 percent. Pseudomonas types were found most frequently and counts varied from more than 1 million to more than 10 million per ml. Flavobacterium sp. was present in an occasional egg in numbers less than 100,000 per ml. Whites and yolks from the initial 550 eggs in group 3 were plated separately. By culturing the white, before the yolk was broken, contamination of the white with yolk was avoided; on the other hand, when the yolk was sampled there was always -a possibility of contaminating yolk with white. However, this did not interfere with the general type of information desired. As shown in Table 3, when cocci were present, they were found in the yolks but not in the whites, while the common

TABLE 3.—Results of culturing whites and yolks separately. Egg stored at 32°F. Number of eggs containing significant numbers of No. of eggs

Micrococci in Yolk

550

8 (5Tto 1 M ave. 200T per ml.)

Streptococci in Yolk

White 0

4 (5M to 50 M per ml.)

White 0

Gram negative rods in Yolk

| White

11 1 11 Chiefly Pseudomonas types (greater than 10 M per ml.)

T=thousand, M =milIion.

spoilage bacteria were present in both yolks and whites in about equal numbers. Group 4 was composed of 168 clean current receipt eggs from a local packing plant (October 1951). The only treatment these eggs received was the usual oiling; they were stored along with group 3 in commercial cold storage. Only 2 eggs of this group contained large numbers of spoilage bacteria. The 180 eggs in group 5 were clean, newly-laid (October 1951) eggs from the College poultry farm. They were held 1 to 2 days in the egg cellar at 59°F., oiled and stored commercially with groups 3 and 4. No eggs in group 5 were found to contain spoilage bacteria when 0.01 ml. quantities of homogenized whites and yolks were plated. In June 1950, 510 clean eggs were collected at the College farm and stored 1 to 2 days in the egg cellar at 59°F. to 64°F. The clean eggs were then artificially soiled by smearing them with a mixture of mud and chicken manure. Twenty-four hours later these eggs were divided into 6 lots which received essentially the same treatments as group 3 eggs. They were stored at 32°F., the same as group 3. At the same time 178 clean eggs were handled in the same manner as group 4 eggs. Examination of these 7 lots of eggs at intervals over a period of 12 months revealed spoilage bacteria in only 6 eggs, with not more than 1 in any single lot. Only 1 of the 688 eggs contained cocci in significant

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a light rainy period in September 1949. Approximately 75 percent were pullet eggs from the range and a majority were smeared with soil. They were stored in an egg cellar at 59°F. to 64°F. for from 1 to 7 days before processing. After washing and treatment, these eggs were stored under the same conditions as group 1 and samples were analyzed periodically during the following 8 months. The percentage of eggs containing large numbers of spoilage bacteria in group 2 was found to be more than twice the number containing comparable numbers of bacteria in group 1.

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MICROBIOLOGY OF DIRTY EGGS

TABLE 4.—Microbial content of eggs stored up to ten months at 42 to 50°F. and a relative humidity of 90 to 100 percent Percent of eggs containing significant numbers of

Group 6. Dirty current receipts (June, 1952, From a local packing plant). No. of Eggs

331 342 360 330 320

Spoilage bact. Treatment

Scrubbed in a detergent Scrubbed in a detergent Dirty Scrubbed in a detergent

Rinsed in water Rinsed in water Not washed Rinsed in water

Scrubbed in a detergent

Rinsed in water

Air dried Air dried "Roccal" (1 oz. to 4 gal. water) Rinsed in 1% NaOH

C. Group 6 (Table 4) A total of 1,683 dirty eggs, sorted from current receipts, were obtained by the case from a local packer during June, 1952. The daily maximum temperature for this period ranged from approximately 90° to 100°F. Four cases of these eggs, excluding "checks," were scrubbed in a detergent, rinsed in water, and variously treated as shown in Table 4. The eggs in one case were allowed to remain dirty. All eggs were stored in a walk-in refrigerator at 42° to 50°F. and 90 to 100 percent relative humidity. After completing the testing of eggs in group 6, at the end of 10 months, it was observed that the number of eggs containing many microorganisms (spoilage bacteria, cocci, etc.) varied from 11 to 33 percent for the different treatments, averaging 22 per cent for all treatments.

Oiled Air dried

Oiled

10 2nd mo. 5 mo. Total

16 12 6 15.5

14 11 10.5 33

19

18.5

Cocci 1st 5 mo.

2nd 10 5 mo. mo. Total

15 11 8 23

3.5 4 0.5 4.2

12 6.5 7 19

19

5

12

8 5 3 10 8

DISCUSSION

Exactly 5,274 eggs (mostly dirties) were processed and examined during this investigation; they were divided into several groups and subjected to various treatments, storage temperatures, and humidities. Since quantitative and qualitative microbiological analyses were made on each egg, this represents a reasonably intensive study. Group 1 eggs, Table 1 were soiled by allowing chickens to run in muddy lots in March 1949. A total of 7 percent of these eggs contained large numbers of spoilage bacteria after periodic analyses over an eight-month storage period at 60°F. to 65°F. A single batch of 100 eggs treated with 2 percent lactic acid for 1 minute, accounted for 3 of the 7 percent containing spoilage bacteria. Six percent of group 1 eggs contained cocci, of which less than one-third showed plate counts of more than 1 million per ml. On the other hand, 16.5 percent of group 2 eggs, Table 1, stored under the same conditions and examined over an eight month period, contained large numbers of spoilage bacteria. This was expected since the eggs were subjected at all times to a temperature favorable for microbial growth (above 60°F.). Furthermore, many of these eggs were collected from the pullet range during an extended

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numbers. On the other hand, 15 percent of 155 clean eggs smeared with millions of psychrophilic Pesudomonas egg-spoilage bacteria and stored under the same conditions (32°F.) were found to contain large numbers of spoilage bacteria. These facts would indicate that the type, the duration, and extent of contamination are important in determining entrance and growth of spoilage bacteria in eggs during storage.

Oiled N o t oiled

1st 5 mo.

740

W. A. MILLER

When 510 clean, one to two day-old June 1950, eggs were dirtied artificially with soil, chicken manure, and known spoilage bacteria, and were allowed to remain dirty only 24 hours, then washed, variously treated and stored at 32°F., only 1.0 percent of the eggs contained significant numbers of spoilage bacteria. Similarly, of 178 clean, one to two day-old June eggs whose only treatment was oiling, only 1 egg (less than 1 percent) had a high count of spoilage bacteria. On the other hand, when the shells of 155 clean, newly-laid, June eggs were artificially coated with millions of psychrophilic Pseudomonas type spoilage bacteria and stored in commercial cold storage at 32°F. and 90 percent relative humidity (same as for the preceding eggs), and examined periodically for 1 year, 15 percent of the eggs contained large numbers of spoilage bacteria (from more than 1 million to more than 10 million Pseudomonas types per ml.). A typical Pseudomonas type organism isolated from 1 of these eggs, when inoculated into a sterile brokenout egg in a sterile jar, caused souring and off odor in 5 days at 54°F. It would appear from the foregoing experiment that the numbers and types of organisms present on the shell at the time the egg goes into cold storage, may play an important role in determining whether or not microorganisms penetrate and grow in the egg. Therefore, from a practical viewpoint, it would seem important that solutions or detergents used in washing dirty eggs should be changed frequently, and that as many microorganisms as possible be removed from the egg shell. Approximately 5 cases (1,683 dirty, current receipt eggs) were purchased from a local packing plant in June 1952. Four cases of these eggs were washed, then each case of eggs treated in a different manner;

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light rainy period in September 1949, and in addition to soil contamination the shells may have remained moist for a considerable time. However, even under these unfavorable environmental conditions 72 percent of these eggs showed no microorganisms on plates containing .01 ml. of homogenized whole egg. When cocci, etc., were included with spoilage bacteria, 28 percent of the eggs contained significant numbers of organisms. In October 1951, 1,200 dirty, current receipt eggs from a local packing plant were divided into 6 equal lots, treated, stored at approximately 32°F., and analyzed over a period of 9 months (group 3, Table 2). Three of these lots of eggs were scrubbed with a detergent and subsequently each batch was treated with a different chemical compound (NaOH, H2SO3, and "Roccal"). An average of 5.5 percent of the eggs in these 3 lots contained large numbers of spoilage bacteria. One lot of eggs scrubbed with a detergent only, one scrubbed with a detergent and thermostabilized in water, and one batch hand buffed, averaged only 1.3 percent of the eggs showing high counts of spoilage bacteria. Only 1 egg of 1,200 had a high mold count while approximately 1.0 percent contained cocci in significant numbers. Groups 4 and 5, Table 2, consisted of 168 clean, current receipts from a local plant, and 180 clean, 1 to 2 day-old, college farm eggs, respectively. These eggs were collected in October 1951, oiled, and stored with group 3 in commercial cold storage. The eggs were cultured over a nine-month period. Only 2 eggs (1.2 percent) in group 4 showed significant numbers of spoilage bacteria, while no egg in group 5 was found to contain spoilage bacteria (.01 ml. of egg plated), although 2.2 percent contained cocci.

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MICROBIOLOGY OF DIRTY EGGS

When gram negative, rod type, "spoilage" bacteria were detected they were usually present in numbers ranging from more than 1 million to more than 10 mil-

lion per ml. Eggs containing more than 1 million cocci per ml. were not ordinarily encountered until after the eggs had been in storage at 59°F. to 64°F. for several weeks or months. The cocci isolated from such eggs showed no growth when incubated for 2 weeks at 41°F. Therefore, cocci can not be considered as a factor causing deterioration of eggs in commercial cold storage (32°F.). In a group of 550 cold storage eggs, Table 3, in which whites and yolks were cultured separately, cocci in significant numbers were found in the yolks but not in the whites of 12 eggs. In 11 eggs from this group, gram negative rod types were found in approximately equal numbers in both yolks and whites. Pseudomonas types were encountered most frequently in eggs from cold storage (32°F.); Flavobacterium was found in an occasional egg. but counts were usually less than 100,000 per ml. ACKNOWLEDGMENT

The author acknowledges the technical assistance of Mr. Byron S. Johnson, and the cooperation of the Poultry Husbandry Department of Kansas State College, Manhattan, and the Perry Packing Company, Manhattan, Kansas. SUMMARY

The data tabulated during this investigation based on bacteriologic analyses of 5,274 eggs indicates that washing dirty eggs in water, a detergent, or a combination of washing and treatment with sodium hydroxide, "Roccal," lactic acid, or sulfurous acid, is no more effective in preventing penetration and growth of spoilage bacteria at a given storage temperature, than storing the eggs dirty or hand buffing them with sandpaper. When 155 clean 1 to 2 day-old eggs were coated with large numbers of psycho-

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the eggs in 1 case were left dirty, and all five cases were stored at 42° to 50°F. Approximately 170 eggs were removed monthly for a period of 10 months, and each egg plated out. The data from group 6 eggs are summarized in Table 4. Only 11 percent of 360 unwashed, dirty eggs contained significant numbers of bacteria, in contrast with 33 percent of 330 eggs that were washed and treated with "Roccal," a quaternary ammonium compound, and oiled; 27 percent of 320 eggs that were washed and immersed in 1 percent sodium hydroxide and oiled; 23 percent of 331 eggs that were washed and oiled; and 16 percent of 342 eggs that were washed but not oiled. In this connection Conner and associates (1953) presented data which indicated that the percent of untreated dirty eggs containing bacteria was no higher than similar groups of variously treated dirty eggs. Of the eggs containing spoilage bacteria in group 6, approximately 25 percent yielded a flora in which coliform bacteria predominated, while Pseudomonas types were encountered most frequently in the remaining 75 percent. In addition, streptococci were present, apparently in pure culture in about one-fourth of the 113 eggs listed in Table 4 as containing cocci in significant numbers. These streptococci were tentatively identified as Streptococcus faecalis, and were usually present in numbers ranging from 5 million to 60 million per ml. of homogenized egg. Micrococci producing white colonies were most frequently observed in the remaining three-fourths of the 113 eggs containing cocci. Plate counts of micrococci were generally below 1 million per ml.

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B. B. RIEDEL

odors, even though plate counts were below 10 million per ml. REFERENCES Conner, J. W., E. S. Snyder and H. L. Orr, 1953. The influence of washing and oiling on grade and bacterial content of eggs stored for a nine month period. Poultry Sci. 32: 227-235. Forsythe, R. H., J. C. Ayres and J. L. Radio, 1953. Factors affecting the microbiological populations of shell eggs. Food Tech. 7:49-56. Funk, E. M., 1948. Experiments in cleaning soiled eggs for storage. Res. Bulletin 426. Missouri Agr. Exp. Sta. Lorenz, F. W., and P. B. Starr, 1952. Spoilage of washed eggs. 1. Effect of sprayed versus static water under different washing temperatures. Poultry Sci. 31: 204-214. Lorenz, F. W., F. X. Ogasawara and P. B. Starr, 1952. Spoilage of washed eggs. 3. A survey of ranch practices and results. Poultry Sci. 31: 221226. Miller, W. A., and L. B. Crawford, 1953. Some factors influencing bacterial penetration of eggs. Poultry Sci. 32: 303-309. Starr, P. B., F. W. Lorenz and F. X. Ogasawara, 1952. Spoilage of washed eggs. 2. Laboratory versus ranch washing. Poultry Sci. 31: 215-220.

The Relationship of Glycine to the Resistance of Chickens to the Roundworm, Ascaridia Galli BERNARD B. R I E D E L

Animal Disease Department, Mississippi State Experiment Station, State College, Mississippi (Received for publication October 23, 1953)

T

HE influence of protein upon the resistance of poultry to helminthiasis was briefly presented in a review by Riedel (1954). Too, Almquist and Grau (1944) found that with respect to growth protein sources may be omitted from the diet of the chick when a mixture of certain amino acids was substituted. From this fact it is reasonable to assume that the increased resistance in animals encouraged by certain protein supplements may be

attributed to specific amino acids rather than the source of protein. The effects of a few amino acids on diseases in poultry have been studied. Briggs, Mills et al. (1942) stated that cystine was instrumental in preventing gizzard erosion in the fowl, and Almquist (1941) noted that choline prevented perosis in chickens. A tryptophane deficiency in chickens was reported by Brown, Wilkening and Schweigert (1948)

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chrophilic Pseudomonas type organisms and stored at 32°F., 15 percent of the eggs contained millions per ml. of the same type bacteria, after periodic examinations over a period of one year. When 526 clean eggs were stored and examined in the same manner, with exception that no bacteria were artificially placed on the shells, only 3 eggs (less than 1 percent) contained significant numbers of bacteria. Eggs which were thermostabilized or pasteurized showed a lower percent containing significant numbers of spoilage bacteria compared with chemically treated eggs in the same group. Organoleptic observations on brokenout eggs indicated that plate counts greater than 10 million per ml. were frequently associated with off odors, while eggs yielding counts below 10 million per ml. usually had no detectable abnormal odors. However, a few eggs containing musty type organisms similar to Pseudomonas graveolens manifested unpleasant