1896 Journal of Food Protection, Vol. 75, No. 10, 2012, Pages 1896–1902 doi:10.4315/0362-028.JFP-11-322 General Interest Evidence for Horizontal and Vertical Transmission in Campylobacter Passage from Hen to Her Progeny N. A. COX,1* L. J. RICHARDSON,1{ J. J. MAURER,2 M. E. BERRANG,1 P. J. FEDORKA-CRAY,1 R. J. BUHR,1 J. A. BYRD,3 M. D. LEE,2 C. L. HOFACRE,2 P. M. O’KANE,2 A. M. LAMMERDING,4 A. G. CLARK,5 S. G. THAYER,2 AND M. P. DOYLE6 1U.S. Department of Agriculture, Agricultural Research Service, Russell Research Center, 950 College Station Road, Athens, Georgia 30605; 2Department Downloaded from http://meridian.allenpress.com/jfp/article-pdf/75/10/1896/1686170/0362-028_jfp-11-322.pdf by guest on 02 October 2021 of Avian Medicine, University of Georgia, Athens, Georgia 30602; 3U.S. Department of Agriculture, Agricultural Research Service, Southern Plains Agricultural Research Center, College Station, Texas 77840; 4Public Health Agency of Canada, 160 Research Lane, Guelph, Ontario, Canada N1G B52; 5University of Toronto, Toronto, Ontario, Canada M5S 1A1; and 6Center for Food Safety, University of Georgia, 1109 Experiment Street, Melton Building, Griffin, Georgia 30223, USA MS 11-322: Received 28 June 2011/Accepted 29 May 2012 ABSTRACT Campylobacter is an important human pathogen, and consumption of undercooked poultry has been linked to significant human illnesses. To reduce human illness, intervention strategies targeting Campylobacter reduction in poultry are in development. For more than a decade, there has been an ongoing national and international controversy about whether Campylobacter can pass from one generation of poultry to the next via the fertile egg. We recognize that there are numerous sources of Campylobacter entryintoflocksof commercial poultry (including egg transmission), yet the environment is often cited as the only source. There has been an abundance of published research globally that refutes this contention, and this article lists and discusses many of them, along with other studies that support environment as the sole or primary source. One must remember that egg passage can mean more than vertical, transovarian transmission. Fecal bacteria, including Campylobacter, can contaminate the shell, shell membranes, and albumen of freshly laid fertile eggs. This contamination is drawn through the shell by temperature differential, aided by the presence of moisture (the ‘‘sweating’’ of the egg); then, when the chick emerges from the egg, it can ingest bacteria such as Campylobacter, become colonized, and spread this contamination to flock mates in the grow house. Improvements in cultural laboratory methods continue to advance our knowledge of the ecology of Campylobacter, and in the not-so-distant future, egg passage will not be a subject continuously debated but will be embraced, thus allowing the development and implementation of more effective intervention strategies. HISTORICAL PERSPECTIVE place and affects the offspring, the acquirement of the disease is by transmission only’’ was disputed, contrary to known Transmission of Campylobacter spp. from the hen to its congenital infections like syphilis (70). This was the attitude progeny in commercial settings is presently debated. The in 1914 when Leo F. Rettger published his seminal paper implication is that the fertile egg can be the site of vertical demonstrating transovarian transmission of Bacterium pull- or transovarian transmission, or for the passage of these orum, the etiological agent of ‘‘white diarrhea,’’ or Pullorum organisms through the shell into the underlying membranes disease, in chickens. Six years earlier, he had published a of the freshly laid, fecally contaminated fertile egg. While article in which he proved the gram-negative bacilli B. vertical transmission is not the only route of Campylobacter isolated from necropsies of affected birds, was contamination for a broiler or broiler breeder flock, it is pullorum, responsible for the disease, fulfilling all of Koch’s postulates definitely one source. On the other hand, many accept that tying a suspect agent to this infection (71). It was noted in certain Salmonella enterica serovars are vertically transmit- earlier work that many of the affected birds failed to absorb ted from parents to offspring. There are several parallels in the yolk sac, a key observation to Rettger’s later 1914 article. our discussions of Campylobacter and vertical transmission with Salmonella and Escherichia coli (7). Leo Rettger was able to isolate B. pullorum, later renamed Salmonella Pullorum, from the yolk sac of chickens with Vertical transmission of an infectious agent, specifically white diarrhea (69). This lead Rettger to the hypothesis that Salmonella Pullorum, was a difficult concept to accept in the parent, particularly the hen, was transmitting the disease 1914. The scientific view then was that infections ‘‘are not to her offspring. Therefore, one would expect to be able inherited,’’ and even the idea that ‘‘germinal infection takes to isolate the pathogen from the ovaries and embryonated eggs in flocks with a history of Pullorum disease, which * Author for correspondence. Tel: 706-546-3484; Fax: 706-546-3772; E-mail: [email protected]. Leo Rettger demonstrated in his 1914 article. He also { Present address: The Coca-Cola Company, 1 Coca Cola Plaza N.W., experimentally infected young chicks with Salmonella Pull- Atlanta, GA 30313, USA. orum and recovered the organisms from the ovaries of those J. Food Prot., Vol. 75, No. 10 CAMPYLOBACTER TRANSMISSION IN EGGS 1897 birds that survived the infection. This approach became the looked. One reason is the difficulty in routinely culturing standard for determining transovarian transmission of an this organism from certain types of samples on a regular infectious agent: isolation of said pathogen from the basis. An ideal cultural procedure for the recovery and reproductive tissue, fertile eggs, and newly hatched offspring. isolation of Campylobacter is not available. Numerous Rettger might have made the fortuitous discovery of vertical plating media, enrichment broths, and procedures have been transmission because the agent Salmonella Pullorum is developed for recovery of Campylobacter. The majority of highly infectious, causes significant mortality, and is these methods were developed for Campylobacter recovery prevalent in tissues of the avian host. Had the first Salmonella from fecal samples in which large populations exist; these proven to be vertically transmitted been Salmonella Galli- methods are not adequate for recovery of small numbers, narum, it might have been harder to prove because of the low sublethally injured or stressed cells, or viable nonculturable prevalence of the pathogen in eggs (56, 61). Salmonella cells (24). Better media and methodological approaches are Pullorum and white diarrhea set the precedent that Salmo- useful to evaluate more fully the ecology of Campylobacter nella could be vertically transmitted in poultry from parents within poultry flocks and routes of transmission. Downloaded from http://meridian.allenpress.com/jfp/article-pdf/75/10/1896/1686170/0362-028_jfp-11-322.pdf by guest on 02 October 2021 to progeny. Another reason why the role of the fertile egg in Salmonella Enteritidis emerged in the 1980s to become Campylobacter transmission has not been fully accepted is the major Salmonella serovar causing human illnesses in the that in some cases, the opposite theory influences experi- United States and Europe (4, 5, 22). An epidemiological mental design and data analysis. Callicott et al. (16) stated link was made between human illnesses attributed to that they could not find any evidence for vertical transmission Salmonella Enteritidis and the consumption of grade A of Campylobacter spp. from grandparent flocks in Sweden table eggs (6, 22, 28, 79). However, screens of table and and their progeny in Iceland, despite Campylobacter from breeder eggs revealed Salmonella Enteritidis prevalence was grandparent birds and the parent birds showing identical low (0.04 to 6.5%) and intermittent, even for Salmonella genetic fingerprints. The authors concluded that this was Enteritidis–positive flocks (42, 43, 68). Even with the because of migrating birds rather than vertical transmission. pooling of eggs (10 eggs per pool), Salmonella Enteritidis However, broiler houses in Iceland are not accessible to the prevalence is low and variable (0 to 8.3%) in positive layer environment, so an influence by wild birds is unlikely. Acuff flocks (39). Similarly, Salmonella Enteritidis prevalence et al. (2) reported that no Campylobacter could be found in rates in the ovaries and oviducts of spent hens have also turkey eggs, but only 20 eggs were tested, and then with insensitive sampling methods. Fonseca et al. (33) sampled the been reported to be low, at 3 and 6%, respectively (68). meconium and a pooled sample of heart, spleen, and liver Experimentally, Salmonella Enteritidis egg transmission is from 117 chicks. When Campylobacter was not isolated, they very low (0.7 to 17%) and intermittent, influenced by many concluded that vertical transmission is a rare event. These factors including immunosuppression, strain type, etc. (34– types of studies leave the impression that the influence of the 37, 50, 62, 66, 77). While colonization of the avian fertile egg in the transfer of Campylobacter is highly reproductive tract with Salmonella Enteritidis is higher improbable. However, there are many reports that support in experimentally versus