Salmonella Gallinarum and Salmonella Pullorum in Poultry: Fowl Typhoid and Pullorum Disease

Introduction

Fowl typhoid and pullorum disease are two distinct but closely related septicemic infections of poultry caused by specific serovars of Salmonella enterica subsp. enterica. Fowl typhoid is caused by Salmonella Gallinarum (a serovar that is nonmotile and lacks flagella) and primarily affects adult chickens, turkeys, and other gallinaceous birds. Pullorum disease is caused by Salmonella Pullorum (also nonmotile) and is predominantly a disease of young chicks and poults. Both serovars are host-adapted to avian species and rarely cause disease in mammals, a critical distinction from the broad-host-range Salmonella serovars associated with human salmonellosis.

The two diseases share many clinical and pathological features, but they differ in age predilection, mortality patterns, and epidemiological transmission routes. Accurate diagnosis depends on distinguishing these serovars from other Salmonella serovars, particularly Salmonella Enteritidis and Salmonella Typhimurium, which have zoonotic potential. This article provides an exhaustive clinical and diagnostic reference for veterinary professionals, focusing on etiology, pathogenesis, clinical presentation, diagnostic methodologies, and control strategies.

Etiology

Salmonella Gallinarum and Salmonella Pullorum are classified within the species Salmonella enterica subsp. enterica based on somatic (O) and flagellar (H) antigen profiles. Both serovars lack flagella and are therefore nonmotile, a trait that aids in their differentiation from most other Salmonella serovars. Their O-antigen groups are as follows:

• Salmonella Gallinarum: O antigen group D1 (O:1,9,12). The lipopolysaccharide structure is similar to that of Salmonella Enteritidis, which has implications for serological cross-reactivity.
• Salmonella Pullorum: O antigen group D1 (O:1,9,12) as well, but can be further subdivided into three biotypes based on fermentation of dulcitol and xylose. Classic biochemical tests reveal that S. Pullorum is negative for dulcitol fermentation and varies in xylose fermentation, whereas S. Gallinarum is positive for dulcitol and typically negative for xylose.

Both serovars are facultative intracellular pathogens. Their virulence is mediated by a combination of type III secretion systems (T3SS-1 and T3SS-2) encoded on Salmonella pathogenicity islands (SPI-1 and SPI-2), as well as fimbrial adhesins and iron acquisition systems. The ability to survive within macrophages and to induce systemic dissemination distinguishes these serovars from non-typhoidal Salmonella serovars that remain confined to the intestinal tract.

The genome of S. Gallinarum harbors the spv (Salmonella plasmid virulence) locus on a large plasmid, which is essential for systemic infection in poultry. S. Pullorum carries a similar but smaller virulence plasmid. Deletion of the spv operon results in marked attenuation in a chicken model.

Epidemiology

Host Range and Susceptibility

The primary hosts for Salmonella Gallinarum and Salmonella Pullorum are chickens (Gallus gallus domesticus) and turkeys (Meleagris gallopavo). Game birds such as pheasants, partridges, guinea fowl, and quail are also susceptible. Ducks and geese show relative resistance, although sporadic infections have been reported.

Age susceptibility is a hallmark of these infections:

• Salmonella Pullorum: Disease is most severe in chicks less than two weeks of age. Mortality can exceed 80% in a naive flock. Adult chickens may be asymptomatically infected and can become carriers, transmitting the organism vertically through eggs.
• Salmonella Gallinarum: Fowl typhoid predominantly affects older birds (growing and adult), although chicks can be infected. Mortality in acute outbreaks ranges from 10% to 80% depending on age, immune status, and management conditions.

Transmission

Transmission occurs via both vertical and horizontal routes. Vertical (transovarian) transmission is critical for the persistence of both serovars in breeder flocks. Infected hens can shed Salmonella in their eggs, either in the yolk or albumen. Chicks hatched from infected eggs may die quickly or become latently infected carriers. Horizontal transmission occurs through ingestion of contaminated feed, water, litter, or fomites. The organisms are shed in feces, and cannibalism of dead birds can amplify spread.

The role of mechanical vectors, including rodents, insects, and wild birds, is well documented. Ectoparasites of Poultry such as the red mite (Dermanyssus gallinae) can carry Salmonella Gallinarum and may serve as reservoirs in endemically infected flocks. See the article on Ectoparasites of Poultry: Dermanyssus gallinae, Ornithonyssus sylviarum, Knemidocoptes mutans, Knemidocoptes gallinae, and Argas persicus – Identification, Life Cycles, and Control for further details on mite involvement.

Geographic Distribution

Fowl typhoid and pullorum disease have been eradicated from commercial poultry in many developed countries through intensive testing and culling programs. However, they remain endemic in parts of Asia, Africa, Latin America, and the Middle East. In regions with limited veterinary infrastructure, the diseases cause substantial economic losses due to mortality, reduced egg production, and trade restrictions.

Pathogenesis

Following oral ingestion, Salmonella Gallinarum and Pullorum survive the low pH of the proventriculus and gizzard. They penetrate the intestinal epithelium via microfold (M) cells and enterocytes in the ceca and ileum. Bacteria are then taken up by intestinal macrophages and translocate to the liver, spleen, and bone marrow via the portal circulation.

The systemic phase of infection is characterized by massive bacterial replication within resident macrophages. The Salmonella pathogenicity island 2 (SPI-2) T3SS is essential for intracellular survival, as it inhibits phagolysosomal fusion and allows bacteria to replicate in the Salmonella-containing vacuole. The ability to cause septicemia and death is directly proportional to the bacterial burden in the spleen and liver.

Tissue damage results from both bacterial cytotoxicity and the host inflammatory response. Fibrinous polyserositis, necrotic hepatitis, and splenitis are typical. In pullorum disease, caseous nodules (typhlitis and hepatitis) are often observed. The release of endotoxin (lipopolysaccharide) contributes to fever, anorexia, and vascular compromise, leading to shock and mortality.

Clinical Signs

Salmonella Gallinarum: Fowl Typhoid

Salmonella Gallinarum fowl typhoid in chickens typically presents as acute septicemia with sudden death. In subacute cases, the following signs are observed:

• Marked depression, huddling, and drooping of wings.
• Anorexia and increased thirst.
• Diarrhea with greenish-yellow or sulfur-colored feces.
• Coma and death within 2 to 5 days.
• In laying hens, an abrupt drop in egg production.
• Chronic infection may result in emaciation and anemia.

Mortality rates are highest in growing and adult birds. Survivors may remain carriers.

Salmonella Pullorum: Pullorum Disease in Chicks

Salmonella Pullorum pullorum disease chicks white diarrhea is the classic presentation. Affected chicks exhibit:

• Acute onset of pasty white diarrhea (urate-containing) that adheres to the vent feathers, causing "pasted vents."
• Weakness, staggering, and chills (chicks huddle near heat sources).
• Respiratory signs (labored breathing) due to caseous pneumonia.
• Opacity of the cornea (rare).
• High mortality beginning at 2 to 5 days of age and peaking by day 10.

In older pullets and adult birds, infection is often subclinical. Carrier hens show no signs but lay infected eggs.

Pathology

Gross Lesions

Fowl typhoid:

• Hepatomegaly with a bronze or copper-green discoloration.
• Splenomegaly. The spleen may be mottled with small necrotic foci.
• Hemorrhagic enteritis, particularly of the duodenum and ceca.
• Petechial hemorrhages on the serosal surfaces and myocardium.
• In chronic cases, fibrinous pericarditis and perihepatitis.

Pullorum disease in chicks:

• Caseous nodules (1–3 mm) in the liver, heart, lung, and cecal walls. These nodules are pathognomonic but not always present.
• Palpable nodules in the myocardium.
• Enlarged and hemorrhagic pancreas.
• Unabsorbed yolk sac with purulent contents.
• White diarrhea leads to dehydration and urate deposits around the vent.

Microscopic Lesions

Histopathology reveals multifocal coagulative necrosis in the liver and spleen with infiltration of heterophils and macrophages. The caseous nodules in pullorum disease consist of necrotic cellular debris surrounded by epithelioid macrophages. In fowl typhoid, Kupffer cell hyperplasia and fibrin thrombi are common.

Diagnostics

A definitive diagnosis requires isolation and characterization of the etiologic agent. The following methods are used.

Bacteriological Culture and Isolation

Samples for culture should be obtained from liver, spleen, bone marrow, and yolk sac (in chicks). Intestinal contents are less reliable because other Salmonella serovars may be present. Tissues are homogenized and pre-enriched in buffered peptone water, then enriched in selective media such as Rappaport-Vassiliadis broth or tetrathionate broth, and plated onto brilliant green agar with sulfadiazine or xylose-lysine-deoxycholate (XLD) agar. Both serovars appear as non-lactose fermenters (pale colonies on MacConkey agar). Nonmotility is confirmed by stab inoculation into soft agar tubes.

Biochemical differentiation from other Salmonella serovars is based on the following:

Serotyping

O- and H-antigen agglutination tests using commercial antisera are required to confirm the serovar. Both serovars react with anti-D1 (O:9) serum. They are nonmotile, so no H-antigen is detected.

Molecular Diagnostics

PCR assays targeting serovar-specific markers are widely used. The glgC gene encoding ADP-glucose pyrophosphorylase shows a deletion in S. Pullorum relative to other serogroup D1 salmonellae, enabling differentiation. Multiplex PCR can simultaneously detect S. Gallinarum and Pullorum using primers for the tyv (dTDP-4-dehydrorhamnose reductase) and sdf genes.

Real-time PCR (qPCR) offers rapid detection directly from organ homogenates. High-throughput sequencing (whole genome sequencing) provides definitive serovar assignment and can track outbreak strains but is not routinely used for single-case diagnostics.

Serology

Serological tests are valuable for flock screening and eradication programs.

• Plate agglutination test (whole blood or serum) using stained antigen (e.g., crystal violet). This test is rapid and inexpensive but can yield false positives due to cross-reactions with Salmonella Enteritidis or other group D salmonellae.
• Tube agglutination test is more specific and quantitative.
• Commercial ELISA kits (enzyme-linked immunosorbent assay) detect antibodies against group D1 LPS. See the article on Enzyme-Linked Immunosorbent Assay (ELISA) for Feline Leukemia Virus for a general discussion of ELISA principles, though the antigen(s) differ.

Interpretation: A positive serological test indicates exposure, not necessarily active infection. Carriers may remain seropositive for months.

Differential Diagnosis

The clinical signs of fowl typhoid and pullorum disease overlap with several other septicemic diseases of poultry.

• Avian highly pathogenic avian influenza (H5N1): causes sudden death and cyanosis; requires molecular detection (see Highly Pathogenic Avian Influenza (H5N1) in Poultry and Wild Birds: Clinical Signs, Transmission Dynamics, and Surveillance Maps).
• Fowl cholera (Pasteurella multocida): also causes septicemia and green diarrhea; identified by bipolar Gram-negative rods on blood smears (see Fowl Cholera in Poultry: Pasteurella multocida Pathogenesis, Clinical Signs, Prevention, Control, and WOAH Classification).
• Avian colibacillosis (Escherichia coli): caseous lesions in pericardium and air sacs (see Escherichia coli in Chickens and Poultry Products: Bacterial Pathogenesis, Contamination Routes, Clinical Signs in Flocks, and Public Health Risks).
• Mycoplasma synoviae and Mycoplasma gallisepticum: cause respiratory signs and synovitis, not the typhlitis of pullorum disease (see Mycoplasma synoviae: Infectious Synovitis in Chickens and Turkeys – Eggshell Apex Abnormalities and Control).
• Histomonas meleagridis (blackhead): causes cecal cores and liver necrosis in turkeys (see Histomonas meleagridis: Blackhead Disease in Turkeys – Hepatic and Cecal Pathology, Diagnosis, and Control).

Diagnostic Workflow

The following Mermaid diagram summarizes the recommended diagnostic algorithm for a flock with suspected fowl typhoid or pullorum disease.

flowchart TD
    A[Clinical signs: septicemia, white diarrhea, mortality], > B[Postmortem examination]
    B, > C[Liver, spleen, bone marrow samples]
    C, > D{Bacteriological culture}
    D, >|Non-lactose fermenter, nonmotile| E[Biochemical & serotyping]
    E, > F{Confirm *S.* Gallinarum or *S.* Pullorum}
    F, >|Gallinarum| G[Report as fowl typhoid]
    F, >|Pullorum| H[Report as pullorum disease]
    D, >|Zoonotic serovar suspected| I[Further serotyping for Enteritidis/Typhimurium]
    C, > J[Molecular PCR / qPCR]
    J, > K{glgC, sdf markers}
    K, > G
    K, > H
    C, > L[Serology (plate agglutination)]
    L, > M[Flock screening: positive indicates exposure]

Treatment and Antimicrobial Resistance

Treatment is rarely curative on an individual bird basis and is not recommended for eradication. Antibiotics may reduce mortality in an outbreak but do not eliminate carrier status. Additionally, antimicrobial use selects for resistant strains.

Drugs that have been used historically include:

• Sulfonamides (e.g., sulfadimethoxine, sulfaquinoxaline): reduce mortality but are bacteriostatic.
• Tetracyclines (e.g., chlortetracycline): moderate efficacy.
• Fluoroquinolones (e.g., enrofloxacin): effective but banned in some countries for poultry due to concerns about resistance.
• Amoxicillin and trimethoprim-sulfonamide combinations.

Antimicrobial susceptibility testing by broth microdilution or disk diffusion is recommended to guide therapy. Available data indicate increasing resistance to tetracyclines and sulfonamides in endemic regions. Multidrug-resistant S. Gallinarum strains have been reported.

It is critical to note that treated birds remain potential carriers, and infected eggs should not be used for hatching. Treatment should be coupled with strict culling of affected pens.

Control and Prevention

Control relies on a combination of biosecurity, eradication of carrier flocks, and vaccination.

Biosecurity

• All-in, all-out management with thorough cleaning and disinfection between flocks.
• Rodent and insect control. The red mite (Dermanyssus gallinae) has been shown to harbor S. Gallinarum (see Ectoparasites of Poultry).
• Quarantine of new birds and testing prior to introduction.
• Use of Salmonella-free feed and chlorinated water.

Eradication Programs

Many national poultry health authorities implement voluntary or mandatory testing programs. The National Poultry Improvement Plan (NPIP) in the United States and similar schemes in Europe require routine serological testing of breeder flocks. All birds that react positively on plate agglutination tests are culled. Hatcheries must be certified free of pullorum disease.

Vaccination

Live attenuated vaccines are available for fowl typhoid, typically using a rough strain of S. Gallinarum (e.g., strain 9R). This vaccine is administered by injection or drinking water to growing pullets. It provides partial protection against clinical disease but does not prevent infection or shedding. Vaccination is uncommon for pullorum disease because the disease is amenable to eradication.

Inactivated (bacterin) vaccines are less effective and are rarely used.

Egg Sanitation

Eggs from infected breeder flocks should not be used for hatching. If salvage is attempted (not recommended), eggs can be fumigated with formaldehyde gas, but this does not eliminate all internal contamination.

Public Health Considerations

Neither S. Gallinarum nor S. Pullorum is considered a significant zoonotic hazard. Unlike S. Enteritidis, these serovars do not cause gastroenteritis in humans. Nevertheless, they have been isolated sporadically from human clinical specimens, often from laboratory workers or persons with close contact to infected birds. The risk is minimal compared to other Salmonella serovars.

This characteristic is important for differentiation from Salmonella in chickens that does have zoonotic risk, as discussed in the article on Salmonella in Chickens: Clinical Signs, Zoonotic Risks, and Diagnostic Differentiation from Other Enteric Pathogens.

References

[1] Gast RK, Porter RE Jr. Salmonella Infections. In: Swayne DE, Boulianne M, editors. Diseases of Poultry. 14th ed. Hoboken: Wiley-Blackwell; 2020. p. 719-753.

[2] World Organisation for Animal Health. Manual of Diagnostic Tests and Vaccines for Terrestrial Animals. Chapter 3.3.11: Fowl typhoid and pullorum disease. Paris: WOAH; 2023.

[3] Barrow PA, Freitas Neto OC. Pullorum disease and fowl typhoid – new thoughts on old diseases: a review. Avian Pathology. 2011;40(1):1-13.

[4] Shivaprasad HL. Fowl typhoid and pullorum disease. In: Saif YM, editor. Diseases of Poultry. 13th ed. Ames: Iowa State Press; 2013. p. 678-693.

[5] Foley SL, Nayak R, Han J, et al. Population dynamics of Salmonella enterica serotypes in commercial egg and poultry production. Applied and Environmental Microbiology. 2011;77(13):4277-4286.