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Epidemiology, oncologic results and risk stratification model for metachronous peritoneal metastases after surgery for pT4 colon cancers: results from an observational retrospective multicentre long-term follow-up study

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Abstract

Purpose

Metachronous peritoneal metastases (MPM) following a curative surgery procedure for pT4 colon cancer is a challenging condition. Current epidemiological studies on this topic are scarce.

Methods

A retrospective multicentre trial was designed. All consecutive patients who underwent operations to treat pT4 cancers between 2015 and 2017 were reviewed. Demographic, clinical, operative, pathological and oncological follow-up variables were included. MPM were described as any oncological disease at the peritoneum, clearly different from a local recurrence. Univariate and multivariate Cox regression models were constructed. A risk stratification model was created on a cumulative factor basis. According to the calculated hazard ratio (HR), a scoring system was designed (HR < 3, 1 point; HR > 3, 2 points) and a scale from 0 to 6 was calculated for peritoneal disease-free rate (PDF-R). A risk stratification model was also created on the basis of these calculations.

Results

Fifty different hospitals were involved, which included a total of 1356 patients. Incidence of MPM was 13.6% at 50 months median follow-up. The strongest independent risk factors for MPM were positive pN stage [HR 3.72 (95% CI 2.56–5.41; p < 0.01) for stage III disease], tumour perforation [HR 1.91 (95% CI 1.26–2.87; p < 0.01)], mucinous or signet ring cell histology [HR 1.68 (95% CI 1.1–2.58; p = 0.02)], poorly differentiated tumours [HR 1.54 (95% CI 1.1–2.2; p = 0.02)] and emergency surgery [HR 1.42 (95% CI 1.01–2.01; p = 0.049)]. In the absence of additional risk factors, pT4 tumours showed 98% and 96% PDF-R in 1-year and 5-year periods based on Kaplan–Meier curves.

Conclusions

Cumulative MPM incidence was 13.6% at 5-year follow-up. The sole presence of a pT4 tumour resulted in high rates of PDF-R at 1-year and 5-year follow-up (98% and 96% respectively). Five additional risk factors different from pT4 status itself were identified as possible MPM indicators during follow-up.

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Data availability

All data and materials have been made publicly available at the Mendeley Data repository and can be accessed at Cerdán Santacruz, Carlos (2022), “Metachronous peritoneal carcinomatosis after pT4 colon cancer patients”, Mendeley Data, V2, https://doi.org/10.17632/k28wpghcts.2

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Acknowledgements

Study collaborators: Dr. Cristina Rihuete Caro, Hospital Universitario Infanta Elena de Valdemoro (Madrid); Dr. Santos Jiménez de los Galanes Marchán, Hospital Universitario Infanta Elena de Valdemoro (Madrid); Dr. Fernando Fernández López, Hospital Clínico de Santiago (Santiago de Compostela, A Coruña); Dr. Manuel Paz Novo, Hospital Clínico de Santiago (Santiago de Compostela, A Coruña); Dr. Francisco Blanco Antona, Complejo Asistencial Universitario de Salamanca (Salamanca); Dr. José Francisco Noguera Aguilar, Complejo Hospitalario Universitario de A Coruña (A Coruña); Dra. María Taboada Ameneiro, Complejo Hospitalario Universitario de A Coruña (A Coruña); Dr. Enrique Moncada Iribarren, Complejo Hospitalario Universitario de Vigo (Vigo); Dra. Inés Aldray Cao, Complexo Hospitalario Universitario de Ourense (Ourense); Dra. Sandra Núñez Fernández, Complexo Hospitalario Universitario de Ourense (Ourense); Dr. Pedro Villarejo, Hospital Fundación Jiménez Díaz (Madrid); Dr. Héctor Guadalajara Labajo, Hospital Fundación Jiménez Díaz (Madrid); Dra. Natalia Uribe Quintana, Hospital Arnau de Vilanova (Valencia); Dra. Zutoia Balciscueta Coltell, Hospital Arnau de Vilanova (Valencia); Dr. Juan Beltrán de Heredia, Hospital Clínico Universitario de Valladolid (Valladolid); Dra. Beatriz de Andrés Asenjo, Hospital Clínico Universitario de Valladolid (Valladolid); Dr. Christian Nuño Iglesias, Hospital de Cabueñes (Gijón); Dra. Paola Lora Cumplido, Hospital de Cabueñes (Gijón); Dr. Jesús Bollo Rodríguez, Hospital de la Santa Creu y Sant Pau (Barcelona); Dra. Marta Pascual Damieta, Hospital del Mar (Barcelona); Dra. Ane Etxart Lopetegi, Hospital Donostia (San Sebastián); Dr. David Ambrona Zafra, Hospital Arnau de Vilanova de Lleida (Lérida); Dra. Silvia Pérez Farré, Hospital Arnau de Vilanova de Lleida (Lérida); Dr. José Manuel Richart Aznar, Hospital Dr. Peset (Valencia); Dra. Nuria Peris Tomás, Hospital Dr. Peset (Valencia); Dra. Mercedes Estaire Gómez, Hospital General Universitario de Ciudad Real (Ciudad Real); Dra. Esther Garcia Santos, Hospital General Universitario de Ciudad Real (Ciudad Real); Dra. Alicia Calero Amaro, Hospital General Universitario de Elche (Alicante); Dr. Luis Sánchez Guillén, Hospital General Universitario de Elche (Alicante); Dra. Virginia Jiménez Carneros, Hospital General Universitario de Getafe (Madrid); Dra. Ainhoa Valle Rubio, Hospital General Universitario de Getafe (Madrid); Dra. Rosángela Obregón Reina, Hospital General Universitario Gregorio Marañón (Madrid); Dra. Paula Dujovne Lindenbaum, Hospital General Universitario Gregorio Marañón (Madrid); Dr. Eduardo de San Pio Carvajal, Hospital Infanta Cristina (Parla, Madrid); Dra. Elena Sagarra Cebolla, Hospital Infanta Cristina (Parla, Madrid); Dr. Ricardo Frago Montanuy, Hospital Universitario de Bellvitge (Barcelona); Dra. Araceli Mayol Oltra, Hospital Provincial de Castellón (Castellón); Dr. Enrique Boldó Roda, Hospital Provincial de Castellón (Castellón); Dr. Joaquín Carrasco Campos, Hospital Regional Universitario de Málaga (Málaga); Dr. Alberto Titos García, Hospital Regional Universitario de Málaga (Málaga); Dra. Estrella Turienzo Santos, Hospital Universitario Central de Asturias (Oviedo); Dra. Isabel Cifrián Canales, Hospital Universitario Central de Asturias (Oviedo); Dra. Arancha Prada, Hospital Universitario de Badajoz (Badajoz); Dra. María Carmona Agúndez, Hospital Universitario de Badajoz (Badajoz); Dr. Manuel Artiles Armas, Hospital Universitario de Gran Canaria Doctor Negrín (Gran Canaria); Dra. Beatriz Arencibia Pérez, Hospital Universitario de Gran Canaria Doctor Negrín (Gran Canaria); Dra. Lara Blanco Terés, Hospital Universitario de la Princesa (Madrid); Dr. Álvaro Gancedo Quintana, Hospital Universitario de la Princesa (Madrid); Dr. José Antonio Rueda Orgaz, Hospital Universitario Fundación Alcorcón (Madrid); Dr. Federico Ochando Cerdán, Hospital Universitario Fundación Alcorcón (Madrid); Dr. Manuel Díez Alonso, Hospital Universitario Principe de Asturias (Madrid); Dra. Remedios Gómez Sanz, Hospital Universitario Principe de Asturias (Madrid); Dr. Juan Ocaña Jiménez, Hospital Universitario Ramón y Cajal (Madrid); Dr. Julio Galindo Álvarez, Hospital Universitario Ramón y Cajal (Madrid); Dra María del Mar de Luna Díaz, Hospital de Pozoblanco (Córdoba); Dr. Enrique Asensio Díaz, Hospital Universitario Rio Hortega (Valladolid); Dr. Fernando Labarga Rodríguez, Hospital Universitario Rio Hortega (Valladolid); Dra. Marta Allué, Hospital Universitario San Jorge (Huesca); Dra. Alejandra Utrilla Fornals, Hospital Universitario San Jorge (Huesca); Dra. Inmaculada Segura Jiménez, Hospital Universitario Virgen de las Nieves (Granada); Dra. Raquel Conde Muíño, Hospital Universitario Virgen de las Nieves (Granada); Dra. Tamara Fernández Miguel, Hospital Universitario Galdakao Usansolo (Bilbao); Dra. Irune Vicente Rodríguez, Hospital Universitario Galdakao Usansolo (Bilbao); Dra. María Conde Rodríguez, Hospital Universitario Lucus Augusti (Lugo); Dra. Laura Ramírez Ruiz, Hospital Universitario Lucus Augusti (Lugo); Dra. Beatriz Moreno Flores, Hospital General Universitario de Albacete (Albacete); Dra. Cristina Camacho Dorado, Hospital General Universitario de Albacete (Albacete); Dr. Juan Torres Melero, Complejo Hospitalario Universitario Torrecárdenas (Almería); Dr. Miguel Lorenzo Liñán, Complejo Hospitalario Universitario Torrecárdenas (Almería); Dra. María Labalde Martínez, Hospital Universitario 12 de Octubre (Madrid); Dr. Francisco Javier García Borda, Hospital Universitario 12 de Octubre (Madrid); Dr. Eduardo Álvarez Sarrado, Hospital Universitario y Politénico la Fe (Valencia); Dra. Vanessa Concepción Martín, Hospital Universitario Nuestra Señora de la Candelaria (Tenerife); Dra. Carmen Díaz López , Hospital Universitario Nuestra Señora de la Candelaria (Tenerife); Dr. Pedro A. Parra Baños, Hospital Universitario Reina Sofía (Murcia); Dr. Emilio Peña Ros, Hospital Universitario Reina Sofía (Murcia); Dra. Mireia Amillo Zaragüeta, Hospital General de Granollers (Barcelona); Dr. Orlando Aurazo, Hospital General de Granollers (Barcelona); Dr. David Alías Jiménez, Hospital Universitario Rey Juan Carlos (Madrid); Dra. Rocío Franco Herrera, Hospital Universitario Rey Juan Carlos (Madrid); Dr. Antonio Ramos Bonilla, Hospital Severo Ochoa de Leganés (Madrid); Dra. Marta Pérez González, Hospital Severo Ochoa de Leganés (Madrid); Dra. Asunción Pérez Sánchez, Hospital Universitario Virgen Macarena (Sevilla); Dr. Javier Valdés Hernández, Hospital Universitario Virgen Macarena (Sevilla); Dra. Laura González Sánchez, Complejo Hospitalario Insular-Materno Infantil (Las Palmas); Dr. Eudaldo López-Tomasetti Fernández, Complejo Hospitalario Insular-Materno Infantil (Las Palmas); Dr. Carlos Fernández Mancilla, Hospital San Juan (Alicante); Dra. Cristina González Prado, Hospital Universitario de Burgos (Burgos); Dr. Guillermo Cabriada García, Hospital Universitario de Burgos (Burgos).

Funding

No fundings were received for the present study.

Author information

Author notes

  1. Carlos Cerdán-Santacruz and Óscar Cano-Valderrama equally contributed to the present work.

Authors and Affiliations

  1. Colorectal Surgery Department, Hospital Universitario de la Princesa, Diego de León, 62, 28006, Madrid, Spain

    C. Cerdán-Santacruz

  2. Colorectal Surgery Department, Complejo Hospitalario Universitario de Vigo, Vigo, Spain

    Ó. Cano-Valderrama

  3. Colorectal Surgery Department, Hospital Reina Sofía, Murcia, Spain

    E. Peña Ros

  4. Colorectal Surgery Department, Hospital de Fuenlabrada, Madrid, Spain

    Á. Serrano del Moral

  5. General Surgery Department, Hospital de Fuenlabrada, Madrid, Spain

    F. Pereira Pérez

  6. Colorectal Surgery Department, Hospital Universitario y Politécnico la Fe, Valencia, Spain

    B. Flor Lorente

  7. Department of General and Digestive Surgery, Bellvitge University Hospital, University of Barcelona and IDIBELL, Barcelona, Spain

    S. Biondo

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  1. C. Cerdán-Santacruz
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Consortia

Collaborating group for the study of metachronous peritoneal metastases of pT4 colon cancer

  • Cristina Rihuete Caro
  • , Santos Jiménez de los Galanes Marchán
  • , Fernando Fernández López
  • , Manuel Paz Novo
  • , Francisco Blanco Antona
  • , José Francisco Noguera Aguilar
  • , María Taboada Ameneiro
  • , Enrique Moncada Iribarren
  • , Inés Aldrey Cao
  • , Sandra Núñez Fernández
  • , Pedro Villarejo
  • , Héctor Guadalajara Labajo
  • , Natalia Uribe Quintana
  • , Zutoia Balciscueta Coltell
  • , Juan Beltrán de Heredia
  • , Beatriz de Andrés Asenjo
  • , Christian Nuño Iglesias
  • , Paola Lora Cumplido
  • , Jesús Bollo Rodríguez
  • , Marta Pascual Damieta
  • , Ane Etxart Lopetegi
  • , David Ambrona Zafra
  • , Silvia Pérez Farré
  • , José Manuel Richart Aznar
  • , Nuria Peris Tomás
  • , Mercedes Estaire Gómez
  • , Esther Garcia Santos
  • , Alicia Calero Amaro
  • , Luis Sánchez Guillén
  • , Virginia Jiménez Carneros
  • , Ainhoa Valle Rubio
  • , Rosángela Obregón Reina
  • , Paula Dujovne Lindenbaum
  • , Eduardo de San Pio Carvajal
  • , Elena Sagarra Cebolla
  • , Ricardo Frago Montanuy
  • , Araceli Mayol Oltra
  • , Enrique Boldó Roda
  • , Joaquín Carrasco Campos
  • , Alberto Titos García
  • , Estrella Turienzo Santos
  • , Isabel Cifrián Canales
  • , Arancha Prada
  • , María Carmona Agúndez
  • , Manuel Artiles Armas
  • , Beatriz Arencibia Pérez
  • , Lara Blanco Terés
  • , Álvaro Gancedo Quintana
  • , José Antonio Rueda Orgaz
  • , Federico Ochando Cerdán
  • , Manuel Díez Alonso
  • , Remedios Gómez Sanz
  • , Juan Ocaña Jiménez
  • , Julio Galindo Álvarez
  • , María del Mar Luna Díaz
  • , Enrique Asensio Díaz
  • , Fernando Labarga Rodríguez
  • , Marta Allué
  • , Alejandra Utrilla Fornals
  • , Inmaculada Segura Jiménez
  • , Raquel Conde Muíño
  • , Tamara Fernández Miguel
  • , Irune Vicente Rodríguez
  • , María Conde Rodríguez
  • , Laura Ramírez Ruiz
  • , Beatriz Moreno Flores
  • , Cristina Camacho Dorado
  • , Juan Torres Melero
  • , Miguel Lorenzo Liñán
  • , María Labalde Martínez
  • , Francisco Javier García Borda
  • , Eduardo Álvarez Sarrado
  • , Vanessa Concepción Martín
  • , Carmen Díaz López
  • , Pedro A. Parra Baños
  • , Emilio Peña Ros
  • , Mireia Amillo Zaragüeta
  • , Orlando Aurazo
  • , David Alías Jiménez
  • , Rocío Franco Herrera
  • , Antonio Ramos Bonilla
  • , Marta Pérez González
  • , Asunción Pérez Sánchez
  • , Javier Valdés Hernández
  • , Laura González Sánchez
  • , Eudaldo López-Tomasetti Fernández
  • , Carlos Fernández Mancilla
  • , Cristina González Prado
  •  & Guillermo Cabriada García

Corresponding author

Correspondence to C. Cerdán-Santacruz.

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The authors of the article do not have any commercial association that might pose a conflict of interest in relation to this article.

Ethics approval

Local Clinical Research Ethics Committee (CREC) from Hospital de la Princesa (Madrid) approval was obtained (04/21-4398). This study is registered with ClinicalTrials.gov, number NCT05300789. No preregistration exists for the reported studies reported in this article.

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Collaborating group for the study of metachronous peritoneal metastases of pT4 colon cancer members are listed in Acknowledgements section.

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Cerdán-Santacruz, C., Cano-Valderrama, Ó., Peña Ros, E. et al. Epidemiology, oncologic results and risk stratification model for metachronous peritoneal metastases after surgery for pT4 colon cancers: results from an observational retrospective multicentre long-term follow-up study. Tech Coloproctol 27, 1025–1036 (2023). https://doi.org/10.1007/s10151-023-02816-z

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