Case Report: Streptococcus suis Human Infections among Pork Consumers in Jeju, South Korea: Zoonotic Threats

ABSTRACT.

Streptococcus suis, a bacterium commonly found in pigs, causes infections in humans through direct contact with infected animals or consumption of contaminated pork products. Recently, a localized outbreak of S. suis infection in humans resulted in three confirmed cases. All three patients had some form of contact with pigs in their medical history. One patient worked at a pig farm, whereas the other two consumed raw pork soup at the same restaurant. The patients were diagnosed with septicemia, subdural empyema, and infectious spondylitis. Streptococcus suis was isolated from their blood. This study was conducted to investigate the clinical features of three patients with S. suis infection and perform a molecular biological analysis of the strains obtained from them. Subsequent investigations highlighted the potential sources for this rare but serious infection and provided insight into preventive measures.

INTRODUCTION

Streptococcus suis is a gram-positive bacterium that causes a primary health challenge in swine and various infectious diseases in humans, including septicemia, meningitis, arthritis, streptococcal toxic shock–like syndrome, and spondylitis.¹ In South Korea, Jeju Island is especially well known to the public for its pork restaurants and processed foods. Pork plays a large part in tourism; therefore, pig farms and pork restaurants are widespread. “Aejeo-Hoe” is a raw meat soup made from the fetus of a pig or piglets and is one of the traditional local foods of Jeju. Three patients infected with S. suis were hospitalized with severe illness, and they had a history of exposure to pigs in the same area. We analyzed the clinical characteristics of these patients and genome sequencing of the etiological strains.

Case 1 was a 67-year-old previously healthy male who presented with a 2-day history of general weakness and fever. He worked as a livestock farmer in Aewol, a region on Jeju Island. The patient had a blood pressure of 88/53 mm Hg, heart rate of 125 beats/minute, respiratory rate of 26 breaths/minute, body temperature of 38.2°C, and a Glasgow Coma Scale score of 15 (4/5/6). Intravenous vasoactive agents were administered, and the patient was admitted to the intensive care unit. Laboratory results revealed leukocytosis, moderate thrombocytopenia, and elevated hepatic transaminase levels (Table 1). On the sixth day of hospitalization, S. suis was isolated from the blood. Treatment began with meropenem (1 g intravenous injection every 8 hours) for 7 days and was then changed to ciprofloxacin (400 mg intravenous injection every 12 hours). The patient was discharged on ciprofloxacin and subsequently revisited the outpatient clinic, achieving full recovery after 14 days.

Table 1.

Characteristics of three patients infected by Streptococcus suis

Characteristics	Patient 1	Patient 2	Patient 3
Age (years)/Sex	67/Male	76/Male	77/Male
History of Contact with Pigs or Pig Products	Worked at Pig Farm	Consumed Raw Soup of Pig Fetus	Consumed Raw Soup of Pig Fetus
Contact Area	Aewol (farm)	Aewol (restaurant)	Aewol (restaurant)
Job	Pig Farmer	Orchard Farmer	Field Farmer
Medical History	Healthy	Hypertension and Diabetes	Diabetes, Angina, and Hyperlipidemia
Isolation of Pathogen	Blood	Blood	Blood
Symptoms on Admission	General Weakness and Fever for 1 Day	Dysarthria and Right-Sided Weakness for a Day	Lower Back Pain and Intermittent Fever for 20 Days
Diagnosis	Septic Shock	Subdural Empyema	Infectious Spondylitis
Definitive Treatment	Meropenem and Ciprofloxacin	Ceftriaxone, Ciprofloxacin, and Burr Hole Operation	Cefazolin, Ceftriaxone, and Levofloxacin
SOFA Score	11	10	0
ICU Admission	Yes	Yes	No
Mechanical Ventilation	Yes	Yes	No
Inotropics	Yes	Yes	No
Duration of Hospital Stay (days)	10	41	23
Outcome	Cured	Cured	Cured
Laboratory Results on Admission (normal range)
WBC (4.0–10.0 × 103/µL)	18.1	11.2	8.0
Hemoglobin (13–17 g/dL)	11.4	14.5	10.4
Platelets (150–450 × 103/µL)	68	25	407
Total Protein (6.7–8.3 g/dL)	5.8	6.8	6.4
Albumin (3.8–5.3 g/dL)	3.3	3.6	3.6
ALP (104–338 U/L)	733	492	352
AST (8–38 IU/L)	860	139	22
ALT (4–44 IU/L)	538	91	22
BUN (8.0–20.0 mg/dL)	42.2	55.1	15.4
Cr (0.60–1.10 mg/dL)	1.29	3.16	0.84
Glucose (70–110 mg/dL)	–	314	169
CRP (0.00–0.30 mg/dL)	11.11	14.68	16.43
ESR (0–9 mm/hour)	23	–	120
PCT (0–0.05 ng/mL)	>100.0	>100.0	–
Lactic Acid (4.5–14.4 mg/dL)	50.0	50.0	–

ALP = alkaline phosphatase; ALT = alanine aminotransferase; AST = aspartate aminotransferase; BUN = blood urea nitrogen; Cr = creatinine; CRP = C-reactive protein; ESR = erythrocyte sedimentation rate; ICU = intensive care unit; PCT = procalcitonin; SOFA = Sequential Organ Failure Assessment; WBC = white blood cell count.

Case 2 was a 76-year-old male who presented with sudden onset of dysarthria and right-sided weakness. He was an orchard farmer. He had consumed Aejeo-Hoe 10 days prior. He had been experiencing headaches and dizziness for 5 days. A brain computed tomography scan revealed an ∼15-mm mixed-type subdural hematoma in the left frontotemporoparietal area. He also presented with a fever (38.1°C). Laboratory tests showed procalcitonin levels of >100 ng/mL and a C-reactive protein (CRP) level of 14.68 mg/dL (Table 1). Brain magnetic resonance imaging (MRI) showed a fluid level in the left posterior subdural space. He was treated with antiepileptic agents and antibiotics and underwent burr hole drainage. Streptococcus suis was isolated from his blood after 7 days. The patient’s condition improved, but he continued to experience neurological sequelae, such as slight hearing difficulty in the left ear and persistent right-sided weakness.

Case 3 was a 77-year-old male field farmer who visited our clinic with lower back pain and an intermittent febrile sensation that had persisted for 20 days. The patient had eaten Aejeo-Hoe several times at a folk restaurant located in Aewol. Spine MRI showed edema and enhancement at levels 2 and 3 of the lumbar spine along both psoas muscles. Blood tests revealed mild anemia and elevated CRP level and erythrocyte sedimentation rate. Cefazolin, 2 g intravenously every 8 hours, was administered for suspected infectious spondylitis. Streptococcus suis was isolated from his blood 5 days later, and the treatment was changed to ceftriaxone (2 g intravenously every 12 hours). The patient’s condition improved without surgery. After 3 weeks, the patient was discharged with oral levofloxacin 750 mg daily.

Table 1 presents the clinical characteristics and laboratory results of these patients. Patient 1 worked at a pig farm located in Aewol, and the other two patients consumed Aejeo-Hoe at folk restaurants in Aewol. Between the fifth and seventh days of hospitalization, S. suis was isolated from the blood. The isolated S. suis strains had the same antibiotic susceptibility patterns; they were sensitive to most antibiotics except clindamycin, erythromycin, and tetracycline.

To accurately compare the genetic similarity of the bacteria isolated from the blood of the three patients using an automated VITEK II system (BioMerieux, Durham, NC), total genomic DNA was extracted from the bacteria using a Solg^™ Genomic DNA Prep Kit (SGD41-C100, SolGent, Daejeon, South Korea) in accordance with the manufacturer’s instructions. Subsequently, next-generation whole-genome sequencing of the extracted bacterial DNA was performed by Theragen Bio (Seongnam-si, Republic of Korea), enabling a detailed genomic comparison of the bacterial isolates from the three patients.

Accurate gene sequence information for these three cases of S. suis was obtained by whole-genome sequencing analysis (Figure 1). In case 1 (JNUH-SS1), genetic sequence analysis revealed high similarity to the ISU2514 strain of S. suis. Conversely, cases 2 (JNUH-SS2) and 3 (JNUH-SS3) exhibited gene sequences that were very similar to those of the ISU2614 strain. The close genetic relationship between the strains found in cases 2 and 3 indicated a likely common source of contamination. In addition, all three cases were identified as serotype 2 and showed close genetic proximity to each other.

Figure 1.

Phylogenetic tree illustrating the relationships among blood-cultured Streptococcus suis strains from our patients and relevant type strains. This comprehensive genomic tree was constructed using a maximum-likelihood approach, derived from the genomic data of 49 different strains. Bar: 0.0005 substitutions per nucleotide position.

Streptococcus suis has 35 serotypes based on their surface capsular antigens.^2,3 Serotype 2 is commonly associated with human and pig diseases.^1–3 A study of the serotype and virulence of S. suis isolated from pigs in Korea showed that serotype 2 was highly pathogenic and more common in the southern region than in the central region of the country.⁴ The three S. suis isolates identified in this study also appeared to be of serotype 2 and were highly pathogenic strains that caused severe clinical symptoms. Moreover, whole-genome sequencing analysis revealed a close genetic relationship between the strains in cases 2 and 3, pointing to a possible common source of contamination, which could be crucial for public health investigations and interventions.

Streptococcus suis typically resides in the upper respiratory tract of symptomless carrier swine, especially piglets, which are the most susceptible.³ This bacterium causes various diseases, including meningoencephalitis, arthritis, pneumonia, and death in pigs and humans. Human infections occur through direct contact with pigs and consumption of pig-derived products or contaminated fresh pork.^5–10 In Korea, only a few cases have been reported.^11–15 This study presents the first reported cases of S. suis infections in humans associated with the consumption of raw pork products in Korea, emphasizing the zoonotic potential of this bacterium.

The mortality rate in human infections with S. suis is approximately 12%.^9,16 Risk factors for human infection with S. suis include raw pork consumption; exposure to pigs or pork; pig-related occupations, such as pig farmers, slaughterhouse workers, meat-processing workers, and veterinarians; and male sex.^3,16–18 In our study, all the patients were male. Our first patient was a pig farmer, whereas the other two were individuals who ate raw pork soup.

Aejeo-Hoe is a unique local food of Jeju Island and is a dish made by grinding unborn (from pregnant sows) or just-born piglets in a blender, adding various seasonings.¹⁹ Interestingly, there are safety warnings about cysticercosis, a parasite associated with consuming raw pork, but there are no warnings regarding S. suis.¹⁹ Some believe that it boosts men’s stamina, whereas others claim that it helps detoxify pesticides from the body. The first case involved a pig farmer who frequently consumed pork but did not consume raw pork products. The second and third cases involved workers in orchard and field farms who consumed Aejeo-Hoe. Although the consumption of local food and tourist curiosity are significant factors, it is important to inform the public about the risk of serious infectious diseases caused by S. suis and caution them about consuming such foods. To date, human S. suis infections on Jeju Island have probably been underestimated, particularly among transient populations. Thus, we emphasize the need for public health centers to continue the surveillance of swine and human S. suis infections and enforce regulations against illegal processing.

This study has some limitations. First, the study’s sample size was limited to only three cases, which may not fully represent the spectrum of S. suis infections in the population. Second, the study focused on a localized outbreak in Jeju Island, South Korea, which may limit its generalizability to other regions or populations with different pork consumption practices and pig farming methods. Third, travel history and detailed dietary habits were not provided in the case descriptions. However, the study addresses a relatively rare occurrence of S. suis infections in humans associated with pork consumption in Jeju Island, which adds to the limited literature. In addition, focusing on a specific region with a distinct cultural and dietary background provides valuable insights into the epidemiology and transmission dynamics of S. suis infections. The use of whole-genome sequencing to analyze the genetic similarity of S. suis strains provides valuable information about the relatedness of the isolates and offers insights into the source of contamination.

CONCLUSION

In conclusion, the cases presented demonstrate the severity of S. suis infections in humans and underscore the importance of rapid diagnosis and appropriate treatment. Molecular analysis provides insights into the genetic relatedness of the strains, aiding in identifying common sources of contamination. Public health efforts should focus on controlling diseases in animal hosts and promoting hygienic practices in pork production and consumption to mitigate the risk of S. suis infections.